1. pets
2. reptiles

REPTILE ASSEMBLAGES AND
AGROFORESTRY IN THE
SOUTHWEST AUSTRALIAN
WHEATBELT
Tiliqua rugosa
Mei Chen Leng (B.Sc. Hons)
This thesis is presented for the degree of
Masters of Science (by research)
of
The University of Western Australia
School of Animal Biology
2015
DECLARATION
The examination of the thesis is an examination of the work of the student. The work must have
been substantially conducted by the student during enrolment in the degree.
Where the thesis includes work to which others have contributed, the thesis must include a
statement that makes the student’s contribution clear to the examiners. This may be in the form
of a description of the precise contribution of the student to the work presented for examination
and/or a statement of the percentage of the work that was done by the student.
In addition, in the case of co-authored publications included in the thesis, each author must give
their signed permission for the work to be included. If signatures from all the authors cannot be
obtained, the statement detailing the student’s contribution to the work must be signed by the
coordinating supervisor.
Please sign one of the statements below.
1. This thesis does not contain work that I have published, nor work under review for
publication.
Student Signature
.
...........................................................................................
2. This thesis contains only sole-authored work, some of which has been published and/or
prepared for publication under sole authorship. The bibliographical details of the work and
where it appears in the thesis are outlined below.
Student Signature
.....................................................................................................................
3. This thesis contains published work and/or work prepared for publication, some of which
has been coauthored. The bibliographical details of the work and where it appears in the
thesis are outlined below. The student must attach to this declaration a statement for each
publication that clarifies the contribution of the student to the work. This may be in the form of a
description of the precise contributions of the student to the published work and/or a statement
of percent contribution by the student. This statement must be signed by all authors. If
signatures from all the authors cannot be obtained, the statement detailing the student’s
contribution to the published work must be signed by the coordinating supervisor.
Student Signature
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ii
ACKNOWLEDGEMENTS
This journey has taken me longer than I expected, but it’s finally over! Thank you to
Jane Prince for stepping-in and sticking with me. I am most grateful for your guidance,
commitment, unyielding support and belief in my capabilities. Without you, I don’t think
I would have ever finished! I am forever indebted to Pauline Grierson (Plant Biology,
UWA) for her invaluable stable isotope collaboration, which helped repackage my
research into a Masters. Thanks to Patrick Smith (ex CSIRO) and Harriet Mills for their
initial help in the early stages of my research. To my wonderful cohort of editors:
Joanne Edmondston (UWA), Ana Hara and Amanda Page, thank you for all your
constructive feedback.
Honorary mentions to my very exceptional field mentor John Ingrim (the curry king!)
and Steve “The Ox” Zabar from CSIRO Sustainable Ecosystem and my very many
volunteers. The field component of this research would not have been possible without
them, it has been a pleasure guys! I must also thank the people who helped confirm my
flora and fauna identifications: Georg Wiehl (CSIRO Sustainable Ecosystem),
Prof. Dale Roberts (UWA), Brad Maryan, Brian Hanich (Western Australian Museum)
and Andras Szito (DAFWA). Thank you to Grzegorz (Greg) Skrzypek (West Australian
Biogeochemistry Centre) for guidance in my stable isotope preparation and sample
analysis.
My gratitude goes out to the property owners who allowed me access to conduct my
research. They are in no particular order: the crew of ‘Dodgey Downs’: Peter Ruland,
Peter Hasslle, Daryl and Tom, David Guille (Forest Products Commission), Stuart
Hocking, Geoff Woodall (UWA Albany), Bernie Masters (BK Masters Associates), Peter
and Jan Morrell, Peter Grimes (Rewards Group) and Michael and Phillipa Page.
Big shout-out to the girls in my office! Thank you for your friendship, support,
understanding, laughter, trips to Broadway, listening and enduring my whinging and
periodic explosive-expletives during the course of my research . Finally, I am most
grateful to my family and friends for all their encouragement, support and belief during
my research. I thank you for putting up with my mood swings and periodic hermit
mannerisms throughout this unforgettable experience.
Funding for this project was provided by: CSIRO Sustainable Ecosystems, Future
Farming Industries CRC Biodiversity Division and the School of Animal Biology at the
University of Western Australia.
iii
SUMMARY
Recent studies into reptile populations in the Australian agricultural landscape have
shown that there is a steady overall decline in reptile abundance and distribution.
However, profitable hardwood perennial plantations have the potential to create
habitats, refuges and corridors for a variety of species. Whether or not reptiles can
recolonise these revegetated areas is dependent on their feeding habits and their
specific habitat requirements.
This thesis aimed to understand the ecological roles reptiles play in agricultural
landscapes, and in particular, determine if profitable hardwood perennial plantations
can enhance reptile biodiversity in the Western Australian (WA) wheatbelt area. Two
approaches were used: 1) Examination of reptile assemblages and their food
resources (i.e. invertebrates) in three habitats: paddocks, sandalwood plantations and
remnant vegetation. 2) Comparison of the similarities and/or differences between
reptile and invertebrate trophic levels through tracing stable isotopes of carbon (C) and
nitrogen (N) amongst the three habitats.
There are five endemic species of sandalwood in Australia and of these, the Western
Australian sandalwood, Santalum spicatum, has commercial significance as it produces
a grade of oil similar to Indian sandalwood, S. album. Santalum spicatum is distributed
throughout the southern semiarid and northern arid areas of WA, hence making it an
ideal profitable perennial crop. The project was restricted to the 300-600 mm rainfall
zone of the WA wheatbelt area. Three locations were selected in the vicinity of Pingelly
(32° 32’S, 117° 05’E), Bokal (33° 26’S, 116° 54’E) and Monjebup (34° 15’S, 118° 33’E).
At each location there were nine sampling sites, consisting of three replicates within
three habitat types; paddock, sandalwood plantation and remnant vegetation.
This study suggests that young sandalwood plantations (<10 years) are not as effective
as remnant vegetation in providing alternative habitat resources for reptiles. However,
young sandalwood plantations (<10 years) do offer an extended resource for
invertebrate
assemblages
over
paddocks.
Potentially,
this
could
encourage
recolonisation of reptile populations into sandalwood plantations. Results from this
study demonstrated sandalwood mixed host plantations can encourage recolonisation
of generalist reptile species. These findings also highlight the potential benefits that
sandalwood plantations with native mixed hosts can have for specialist reptile species,
as these were shown to be confined to the plantations and remnant vegetation. As
these plantations mature, they will develop in structure, understorey and vegetation
iv
diversity. Thus providing future extended habitat for existing reptile populations in
agricultural lands.
Stable isotope analysis from this study revealed very little difference in the C and N
values between the three different habitats. There was only a slight enrichment in
trophic level in the sandalwood plantation followed by paddock and then remnant
vegetation. Trophic level analysis of the generalist skink, Menetia greyii, revealed no
differences in trophic position between the three habitats. However, M. greyii appeared
to show a dietary shift amongst the three habitats, switching from a carnivorous diet in
more complex habitats (i.e. remnant vegetation) to an omnivorous diet in less complex
habitats (i.e. paddocks and sandalwood plantation). The dietary shift in M. greyii
demonstrates the conservation value of retaining remnant vegetation in agricultural
lands.
Generalist reptile species can be further utilised to investigate the viability of
agroforestry plantations in sustaining reptile populations. Long-term monitoring of reptile
populations as sandalwood plantations age is needed, especially during and after
harvest. Through monitoring we can clarify if these agroforestry plantations can sustain
existing reptile populations and encourage recolonisation of cryptic and specialised
reptile species. Only then, can we aim to appropriately implement management
strategies and policies to help conserve biodiversity in agricultural landscapes.
v
TABLE OF CONTENTS
Page
Declaration: ............................................................................................................... ii
Acknowledgements: ................................................................................................ iii
Summary: ................................................................................................................. iv
Table of Contents: ................................................................................................... vi
List of Figures: ....................................................................................................... viii
List of Tables: .......................................................................................................... ix
Chapter 1: General Introduction
Biodiversity decline in the Western Australian wheatbelt ................................... 2
Fauna and Western Australian agriculture ........................................................ 3
Agricultural revegetation and agroforestry ........................................................ 6
Santalum spicatum R.Br. in Western Australia agriculture ................................ 9
Project approach and aims ............................................................................. 12
Chapter 2: Reptile and invertebrate assemblages in southwest Australia
Reptile and invertebrate assemblages in southwest Australia: a comparison between
sandalwood plantations, native and agricultural ecosystems.
Abstract .......................................................................................................... 14
Introduction ..................................................................................................... 14
Methods .......................................................................................................... 16
Study site and sampling design .................................................................. 16
Sample collection ....................................................................................... 17
Data analysis ............................................................................................. 19
Results ........................................................................................................... 20
Discussion ...................................................................................................... 30
vi
Chapter 3: Reptile trophic structure in sandalwood agroforestry
Trophic relationships of Menetia greyii in sandalwood plantations compared to native
and cropped ecosystems in Southwest Australia.
Abstract .......................................................................................................... 36
Introduction ..................................................................................................... 36
Methods .......................................................................................................... 39
Study site and sampling design .................................................................. 39
Collection of plant, invertebrate and M.greyii samples ................................ 40
Stable isotope analysis .............................................................................. 41
Data analysis ............................................................................................. 41
Results ........................................................................................................... 42
Discussion ...................................................................................................... 47
Chapter 4: General Discussion ............................................................................. 50
References ............................................................................................................. 56
Appendices
Appendix I: Stable isotope analysis of samples ........................................................ 69
Appendix II: Stable isotope means (± SE) across the three habitats ........................ 70
Appendix III: Stable isotope means (± SE) across the three study areas ................. 71
vii
LIST OF FIGURES
FIGURE 1: Percentage of pre-European vegetation currently remaining in Australia.
of the Environment Report (2011).
FIGURE
2:
Western
Source: State
......................................................................................... 3
Australia
distribution
of:
(a)
Egernia stokesii
badia
and
(b) Cyclodomorphus branchialis Source: Atlas of Living Australia website at http://www.ala.org.au. Access
online 31 July 2014.
.......................................................................................................... 4
FIGURE 3: Region of 300-600 mm rainfall zone (in green) in the Western Australian wheatbelt,
where agroforestry schemes are most successful. ............................................................ 8
FIGURE 4: (a) 4-5 year old Santalum spicatum in a south-western Australian plantation.
(b) Santalum spicatum fruit. ......................................................................................... 10
FIGURE 5: The distribution of Santalum spicatum in Australia.
Source: Geoff Woodall, Centre of
Excellence in Natural Resource Management, University of Western Australia, 2011.
.......................... 10
FIGURE 6: South-western Australia, showing wheatbelt area (brown), location of study sites
(blue), surrounding cities and towns (black) and major roads (yellow). Source: DAFWA 2010 and
Google Earth 2014.
......................................................................................................... 18
FIGURE 7: CAP ordination plot relating reptiles to habitat: paddock (Pad), sandalwood (San)
and remnant (Rem) and location (based on Bray Curtis after square root transformation, vector
overlay of habitat association of dominate reptile species based on Spearmen’s correlation
>0.6). ......................................................................................................................... 23
FIGURE 8: CAP ordination plot relating invertebrates to habitat: paddock (Pad), sandalwood
(San) and remnant (Rem) and location (based on Bray Curtis after Log(X+1) transformation,
vector overlay of habitat association of dominate invertebrate orders based on Spearmen’s
correlation >0.6). ......................................................................................................... 27
FIGURE 9: DistLM plot for reptile data using the ‘BEST’ selection procedure on the bases of the
AIC selection criterion (based on Bray Curtis after square root transformation), overlaid with
invertebrate data. Pad = Paddock, San = Sandalwood, Rem = Remnant. ........................... 29
viii
FIGURE 10: Plot of combined mean δ15N against δ13C (± SE) of trophic composition of
secondary consumers in three habitats within study locations (a) Pingelly, (b) Bokal,
(c) Monjebup., NHV-Non herbaceous vegetation, HV-Herbaceous vegetation, LL Leaf litter,. IH
Invertebrate herbivore, IC-Invertebrate carnivore, IO Invertebrate omnivore. ...................... 43
LIST OF TABLES
TABLE 1: Mean (± SE) number of reptile species per site caught across the three different
habitats (Pad = Paddock, San = Sandalwood, Rem = Remnant) at each location: Pingelly, Bokal
and Monjebup over the active reptile periods Feb-Mar 2009, Nov-Dec 2009 and Jan-Feb 2010.
Life guilds: Terrestrial (t), Fossorial (f), Saxicolous (s) and Arboreal (a). ............................ 21
TABLE 2: Permutational multivariate analysis of variance based on Bray-Curtis similarities
testing the effect of location and habitat on reptile assemblage structure. P≤0.05*, P≤0.0001***.
.................................................................................................................................. 22
TABLE 3: Pair-wise post-hoc analysis of reptile assemblages based on Bray-Curtis similarities
(a) between locations and (b) between habitats. P = Pingelly, B = Bokal, M = Monjebup.
Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*, P≤0.001**. ...................... 22
TABLE 4: (a) Mean (± SE) number of reptile abundance and species richness (number of
habitat per site). Numbers were summed across three sites in each habitat at each
location and averaged across location for each habitat. (b) Unvariate pair-wise post-hoc
analysis of reptile species richness based on Euclidean distance between habitats.
Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*. ...................................... 24
TABLE 5: Mean (± SE) number of invertebrates per site, grouped by order, trapped over a one
week period in the months November 2009 and January 2010. The order Hymenoptera was
separated into ants and wasps and bees. Pad = Paddock, San = Sandalwood, Rem = Remnant.
.................................................................................................................................. 25
TABLE 6: Permutational multivariate analysis of variance based on Bray-Curtis similarities
testing the effect of location and habitat on invertebrate assemblage structure. P≤0.001**.
.................................................................................................................................. 26
ix
TABLE 7: Pair-wise post-hoc analysis of invertebrate assemblages based on Bray-Curtis
similarities (a) between locations and (b) between habitats. P = Pingelly, B = Bokal, M =
Monjebup. Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*, P≤0.001** ......... 26
TABLE 8: (a) Mean (± SE) number of invertebrate abundance and invertebrate order richness
(number of habitat per site). Numbers were summed across three sites in each habitat
at each location and averaged across location for each habitat.. (b) Unvariate pair-wise
post-hoc analysis of invertebrate abundance and order richness based on Euclidean distance
between locations and between habitats. P =
Pingelly, B =
Bokal, M =
Monjebup.
Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*. ....................................... 28
TABLE 9: Result summary of reptile and invertebrate abundance, richness and assemblages.
Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*, P≤0.001**. ...................... 30
TABLE 10: Permutational analysis of variance based on Euclidean distance, testing the effect of
15
location and habitat on δ N values. P≤0.05*, P≤0.001**, P≤0.0001***, df = degrees of freedom.
.................................................................................................................................. 44
TABLE 11: Pair-wise post-hoc analysis within the interaction between location and habitat for
15
δ N values of vegetation a) between locations within habitats and b) between habitats within
locations. P = Pingelly, B = Bokal, M = Monjebup. Pad = Paddock, San = Sandalwood, Rem =
Remnant. P≤0.05*, P≤0.001**, P≤0.0001***. .................................................................. 45
TABLE 12: Pair-wise post-hoc analysis of invertebrate δ15N values on Euclidean distance-based
similarity matrix between locations and between habitats (a) Invertebrate Herbivore,
(b) Invertebrate Omnivore. Pad = Paddock, San = Sandalwood, Rem = Remnant. P = Pingelly,
B = Bokal, M = Monjebup. P≤0.05*, P≤0.001**, P≤0.0001***. ........................................... 46
TABLE 13: Pair-wise post-hoc analysis within the interaction between location and habitat for
15
δ N values of M. greyii a) between locations within habitats and b) between habitats within
locations. P =
Pingelly, B = Bokal, M = Monjebup. Pad = Paddock, San =
Sandalwood,
Rem = Remnant. P≤0.05*, P≤0.001**. Probabilities are taken from Monte Carlo simulations.
.................................................................................................................................. 47
x
CHAPTER 1
GENERAL INTRODUCTION
Western Australian sandalwood (Santalum spicatum) 1-2 year old plantation. Lighter green
vegetation is the sandalwood plantation, dark green vegetation is surrounding natural
bushland and brown areas are agricultural lands.
BIODIVERSITY DECLINE IN THE WESTERN AUSTRALIAN WHEATBELT
The decline of biodiversity is a critical environmental issue facing Australia and the
world. One the major contributors towards diminishing biodiversity is land clearing,
much of this land modification occurs in the agricultural regions, causing detrimental
effects on their ecosystems and hence impacting on rural biodiversity (Bartle et al.
2002; Hobbs et al. 2003b). Pastures and crops occupy approximately 37% of global
land use, often resulting in altered landscape structure and function, as well as
contributing significantly to global deforestation (Bowen et al. 2007). Such large-scale
land clearing is having a profound effect on the distribution of native vegetation,
resulting in a devastating effect on biodiversity and ecosystem processes in the
agricultural region (Hobbs et al. 2003b; Vesk & Mac Nally 2006). This has raised
questions in regards to the ability for species and communities to persist in the
changed landscape dominated by agriculture (Saunders et al. 1991).
The wheatbelt region of Western Australia (WA) has long been subjected to broadscale vegetation clearing. The WA wheatbelt is an area that covers approximately 15%
of the State, in a broad band east of Perth, spanning from Geraldton to Esperance. The
2007 Western Australian State of Environment Report, released by the Environmental
Protection Authority (EPA), stated that the wheatbelt is the most stressed region in WA
with over 90% of its original vegetation cleared (Figure 1). This has resulted in remnant
vegetation left as either small isolated pockets that are of poor quality, as discontinuous
narrow strips along roadsides and drainage systems, or as single trees in paddocks
(Hobbs 1993; Majer et al. 2001; EPA 2007).
2
FIGURE 1: Percentage of pre-European vegetation currently remaining in Australia.
Source: State of the Environment Report (2011).
FAUNA AND WESTERN AUSTRALIAN AGRICULTURE
Of the original mammalian fauna known from the wheatbelt, 18 species have become
extinct and only 10 species remain in the remnant vegetation (Kitchener et al. 1980b).
The avian fauna has fared better, with only two species of 148 becoming extinct in the
past 80 years (EPA 2007). Of the non-perching birds in the wheatbelt, 43 of the
139 species have declined in range and/or abundance and only three of these birds
have increased in range and/or abundance (Saunders 1993). Of the reptile species
currently found in the wheatbelt region, the Environmental Protection and Biodiversity
Conservation Act (1999) lists only one species, Western spiny-tailed skink
(Egernia stokesii badia) as endangered, having a narrow distribution starting from
Mullewa and extending south to Kellerberrin (Figure 2).
3
Another reptile species classified as rare, with the possibility of becoming extinct, is the
Gilled slender bluetongue (Cyclodomorphus branchialis). This is due to its confinement
in the northern wheatbelt, ranging from the Murchison and Irwin River area and
extending inland to Mount Magnet (Bush et al. 2007, Figure 2). The Western Australian
Wildlife Conservation (Specially Protected Fauna) Notice 2008 (2) currently lists the
Woma or Sand python (Aspidites ramsayi) under specially protected fauna, although it
is most likely extinct. Aspidites ramsayi was once widespread in the southwest
wheatbelt region. However, clearing has seen a dramatic decline in numbers since
1960, with the last sighting in 1989 (Bush et al. 2007).
(a)
(b)
FIGURE 2: Western Australia distribution of: (a) Egernia stokesii badia and (b)
Cyclodomorphus branchialis
Source: Atlas of Living Australia website at http://www.ala.org.au. Access
online 31 July 2014.
4
There is little knowledge of the ecological benefits of revegetation in agricultural land
(Vesk & Mac Nally 2006), with limited research on habitat resources provided for fauna
(Hobbs et al. 2003a). Despite this, the use of native species as hardwood perennial
crops in agroforestry ventures could assist in maintaining, and potentially enhance, rural
biodiversity. These hardwood perennial plantations could create alternative habitats,
refuges and corridors for a variety of species. This could be important for various flora
and fauna that may not otherwise survive in an agricultural landscape (Baudry et al.
2000).
The general consensus of reptiles being able to better adapt to landscape
modifications, compared to other taxa (Kitchener et al. 1980a; Burbidge & McKenzie
1989) is mostly accredited to their low energy and space requirements (Turner et al.
1969). Despite this, recent studies into reptile populations in the Australian agricultural
landscape have shown that there is a steady overall decline in reptile abundance and
distribution (Sarre et al. 1995; Smith et al. 1996; Sarre 1998; Mac Nally & Brown 2001;
Driscoll 2004). These findings further support the concept that reptiles are
characteristically sedentary and of low mobility and hence, may be susceptible to
disruptive ecosystem changes (Fischer et al. 2003; Driscoll 2004; Fischer et al. 2004).
Whether or not reptiles can recolonise revegetated areas depends on their feeding
habits and specific habitat requirements. For example, Cunningham et al. (2007) found
Southern marbled gecko (Christinus marmoratus) and Southern rainbow skink
(Carlia tetradactyla) to be more abundant in seedling re-growth than coppice re-growth.
However, C. marmoratus favoured seedlings in perennial plantings and C. tetradactyla
favoured native remnant seedlings and tussock grass cover. Carnaby’s wallskink
(Cryptoblepharus carnabyi) on the other hand, was found more abundant on coppice
re-growth compared to seedling re-growth; and Boulenger’s skink (Morethia
boulengeri) was dependant on specific habitat conditions and was therefore more
prolific in plains.
Another factor affecting reptile re-colonisation is the age of the vegetation. Nichols and
Bamford (1985) found that 4-6 year old revegetated bauxite mine sites had some
capacity to support reptile species similar to those reptile species found in poor quality
remnant vegetation. However, a study by Nichols and Nichols (2003) found the
diversity of reptile species in eight-year-old rehabilitated mine sites was still low
compared to unmined sites. This suggests it may take years before revegetated sites
are able to support a wider variety of reptile species. Munro et al. (2009) suggested
5
that it may take as long as 30-40 years for revegetated agricultural areas to begin to
resemble surrounding remnant vegetation. Even after this period of time, native ground
cover is still absent and structural diversity such as fallen logs, tree hollows and deep
leaf litter have only just begun to develop.
Reptiles may provide a solution to measuring biodiversity change as they are a major
component of the vertebrate diversity in the WA wheatbelt (D. Roberts, pers. comm.).
The 2008 Western Australian Wheatbelt Oil Mallee Biodiversity project, led by Future
Farming Industries Salinity Cooperative Research Centre, indicates that reptiles may
show a successional pattern of re-colonisation on farmland re-planted with perennial
vegetation (F.P. Smith, pers. comm.). In addition, a forestry study conducted by
Goodall et al. (2004) concluded that reptiles respond to harvesting disturbance and
post-harvest successional stages of regeneration. Skinks associated with the ‘bark, log
and rock dwelling’ guild (Lampropholis spp. and Carlia spp.) appeared to act as
surrogates for the presence or absence of other species. Although Goodall et al. (2004)
looked at forestry ecosystems, profitable hardwood perennials in agricultural
landscapes may have some similarities. Hence, members of the Scincidae family may
be good candidates to assess and measure biodiversity in an agricultural landscape.
AGRICULTURAL REVEGETATION AND AGROFORESTRY
The intensification of land degradation in the agricultural zone of WA has prompted
community involvement in revegetation over the past 20 years. This has been
supported by agro-environmental incentives (such as Landcare) to address
environmental degradation and move towards sustainable farming practices (Vesk &
Mac Nally 2006). The aim of these schemes is to reverse some of the environmental
damage caused by agricultural intensification and, by doing so, ensure a sustainable
farming future, mostly through vegetation restoration (Donald & Evans 2006).
While revegetation occurring in the agricultural zone of the southwest Australia serves
a number of purposes such as salinity control or shelter for stock, one of the key goals
is the conservation of native biodiversity (Vesk et al. 2008). However, many of the
revegetation schemes are small and isolated from remnant vegetation patches and
have high perimeter to area ratios, rendering them insufficient for the re-establishment
of fauna (Freudenberger et al. 2004; Radford & Bennett 2007). These unconnected,
scattered, small patches of revegetation add little to the existing landscape vegetation
and are often ideal for problem species such as feral or pest animals (e.g. foxes and
6
mice) and weeds, which negatively impact conditions for the majority of declining fauna
existing in the agricultural landscape (Vesk & Mac Nally 2006).
To address these issues that have arisen from past agricultural revegetation and to
offer profitable incentives for farmers, at the same time enhancing WA’s rural
biodiversity, there has been an increase in agroforestry ventures. Agroforestry is a
farming system that involves the combination of hardwood perennials and herbaceous
crops, with or without livestock (Torres 1983). Although its main purpose is to control
dry-land salinity (Lefroy et al. 2005), these plantations also function as shelter for stock
and can be an alternative source of income through the commercialisation of native
hardwood perennials (e.g. acacia, sandalwood and oil mallee).
Whilst these agroforestry ventures can be highly successful, they will not come to
dominate farmland use. This is due to a combination of factors such as soil type and
constraints on machinery, labour availability and economic risk considerations
(Bathgate & Pannell 2002). Most agroforestry ventures depend on the success of the
plantation and its economic performance. Due to their commercial potential and the
need to maximise profits, plantations are often limited to regions associated with higher
rainfall (Bathgate & Pannell 2002). For the WA wheatblet this area is restricted to
mainly the 300-600 mm rainfall zone of the southwest, spanning from the town of
Pingelly south towards Borden (Figure 3).
7
FIGURE 3: Region of 300-600 mm rainfall zone (in green) in the Western Australian
wheatbelt, where agroforestry schemes are most successful.
8
Bartle et al. (2002) recognised the potential for the wheatbelt region to develop three
types of hardwood perennial crops:
1. Short-rotation coppice crops: Evolved from the Oil Mallee Project, these crops
are harvested every 2-5 years and successive crops are regenerated from
rootstock. These crops are ideal along contours and other locations to intercept
downslope water runoff.
2. Short-rotation phase crops: These crops are integrated within the annual crop
rotation in paddocks and are harvested once and removed at the age of 3-6 years.
These crops (e.g. acacia) can have the potential to dewater productive land and
therefore, hinder the yield of following annual crops.
3. Long-rotation crops: These crops have a production cycle greater than 10 years
and may be longer than 100 years (e.g. sandalwood). They are best suited to the
wetter wheatbelt regions due to higher growth rates and planted in belts or small
blocks.
SANTALUM SPICATUM R.BR. IN WESTERN AUSTRALIAN AGRICULTURE
One agroforestry system that has been established in WA for more than 150 years
involves the cultivation of native sandalwood. Cultivation of this hardwood perennial is
mainly in standalone crops. However it can be in combination with herbaceous crops,
with or without livestock. Santalum spicatum is an indigenous Australian sandalwood
species (Figure 4). It is a small-growing tree, reaching heights of 5-20 m. It is also a
root hemi-parasite that relies on a host plant for sustenance throughout its life (Shobha
1990; Hettiarachchi et al. 2010).
Natural and cultivated stands of S. spicatum cover a large proportion of Australia
(Figure 5) and like Indian sandalwood (S. album) it has historically been a wild-sourced
product. The majority of Australia’s sandalwood cover is in WA, with over 42 million ha
of S. spicatum growing in the State (Tonts & Selwood 2003). Its aromatic wood and oil
is highly valued and is used to produce a number of products including incense sticks,
ornaments and cosmetics. Commercial export of WA sandalwood dates back to 1845,
when five tonnes was first exported from the port of Fremantle to Ceylon (Tonts &
Selwood 2003).
9
(a)
(b)
FIGURE 4: (a) 4-5 year old Santalum spicatum in a south-western Australian plantation.
(b) Santalum spicatum fruit.
FIGURE 5: The distribution of Santalum spicatum in Australia. Source: Geoff Woodall, Centre of
Excellence in Natural Resource Management, University of Western Australia, 2011.
10
Land clearing in the 19th and early 20th centuries resulted in an enormous growth of
sandalwood supply for WA, which primarily provided the State’s highest source of
foreign income to the new colony (Hettiarachchi et al. 2010). Seeing the value of
sandalwood, the Western Australian State Government took measures to protect the
species through control harvesting by passing the Sandalwood Control Act (1929).
Today the regulation of the sandalwood industry is managed by Department of Parks
and Wildlife (DPaW; formerly Department of Conservation and Land Management) who
is responsible for administrating the Sandalwood Control Act (1929), which still applies
today and is regulated by the Forest Product Commission (FPC).
Since 1987 the FPC and DPaW successfully established S. spicatum plantations
throughout the medium annual rainfall area (400-600 mm) of the WA wheatbelt, with
the aim of supplementing the harvest of natural stands of sandalwood with plantation
timber (Clarke 2006). Over the past 10 years, S. spicatum plantations have increased
to over 10 000 ha. With the current rate of planting, it is estimated that by the year 2020
there will be 50 000 ha of sandalwood plantations in Australia (Rao et al. 2011).
Currently, WA supplies approximately 50% of the global demand for sandalwood
(Hettiarachchi et al. 2010).
11
PROJECT APPROACH & AIMS
The objective of this project was to understand what contribution profitable hardwood
perennial farming systems, in this case sandalwood plantations, can make to the
conservation of reptile biodiversity in the wheatbelt area. One of the challenges of this
project was to measure change in ‘biodiversity’ in response to changes in the
agricultural system and landscape. To do this, I measured the abundance and diversity
of reptile assemblages in paddock, sandalwood plantations and remnant vegetation
and compared their trophic structure between those habitats. It was anticipated that
results from this study would contribute towards the development of an assessment
system that would allow farmers and land managers to rapidly assess and monitor the
developing health of ecosystems on their properties in response to increased profitable
perennial farming systems. The two main hypotheses of this study were:
1. Reptile assemblages in sandalwood plantations and remnant vegetation will
have similar abundances, with lower abundance in paddocks and will be more
diverse than those on cleared agricultural land. To assess this I compared
reptile assemblages between three habitat types: paddocks, sandalwood
plantations and remnant vegetation. In addition, food resources for reptiles
(i.e. invertebrates) were also investigated for variation in abundance and
diversity between paddocks, sandalwood plantations and remnant vegetation.
2. Sandalwood plantations provide better habitat support for reptiles than
paddocks and will have the same level of habitat support for reptiles as remnant
vegetation. This was assessed by comparing the assemblages of potential prey
items among habitats and comparing similarities and/or differences between
trophic levels through tracing carbon (C) and nitrogen (N) stable isotopes.
12
CHAPTER 2
REPTILE AND INVERTEBRATE
ASSEMBLAGES IN
SOUTHWEST AUSTRALIA
Clockwise from top left hand corner: Diplodactylus granariensis, Pogona minor,
Ctenotus impar, Underwoodisaurus milli, Liopholis multiscutata, Ramphotyphlops australis,
Morethia obscura, Parasuta gouldii and Eremiascincus richardsoniiI (center).
REPTILE AND INVERTEBRATE ASSEMBLAGES IN SOUTHWEST AUSTRALIA: A
COMPARISON BETWEEN SANDALWOOD PLANTATIONS, NATIVE AND
AGRICULTURAL ECOSYSTEMS
ABSTRACT
Sandalwood plantations on farms may provide habitat resources for native reptiles and
their food source i.e. invertebrates. By providing additional refuge, sandalwood
plantations may also improve reptile persistence in farmland. Reptile and invertebrate
assemblages in remnant vegetation, sandalwood plantations and cropping paddocks
were compared in three different areas in the wheatbelt of southwest Australia. Reptile
assemblages in remnant vegetation were different to those in the sandalwood
plantation and paddock. Although mean reptile abundance per site was similar across
the three habitats, species richness was higher in remnant vegetation (8.44 ± 1.094)
followed by sandalwood plantation (4.89 ± 0.59) and then paddock (3.5 ± 0.42).
Invertebrate assemblages were different across the three habitats. Invertebrate mean
abundance per site was greater in sandalwood plantation (7.34 ± 0.15) than paddock
(6.15 ± 0.27) and slightly higher in sandalwood plantation than remnant vegetation
(7.30 ± 0.53). Invertebrate order richness was higher in remnant vegetation (10 ± 0.50)
followed by sandalwood plantation (8.9 ± 0.35) and then paddock (7.9 ± 0.48). Results
suggest invertebrate assemblages increased in diversity when paddocks are planted
with sandalwood, whilst reptile assemblages are slower to recover. While young
sandalwood plantations may not provide the same habitat resources as remnant
vegetation, they appear to provide a better habitat than paddocks for invertebrates and
possibly for reptiles in the future. As these sandalwood plantations mature they may
play a role in maintaining and increasing invertebrate species diversity in agricultural
lands, which in turn may benefit reptiles.
INTRODUCTION
Habitat components of woodlands such as logs and leaf litter are all necessary for
sustaining reptile populations. The structural complexity of vegetation and habitat
components near ground level are important refuges for numerous reptiles such as
skinks, legless lizards, geckos and elapid snakes (Brown 2001). Fischer et al. (2004)
found that reptile species richness increased as the structural diversity of habitats
increased. As habitats become more structurally complex over time, additional
14
resources develop, such as increased shelter and nesting sites, and a greater
abundance of prey items. However, these ground layer microhabitats are particularly
sensitive to land degradation (Dorrough et al. 2012).
In an agricultural setting, land degradation can arise from livestock grazing, timber
harvesting, firewood collection, soil compaction and weed invasion (Brown 2001).
These disturbances may cause disruptions or changes in reptile biology, behaviour and
interactions with other species, resulting in a possible decrease in reptile diversity
(Fischer & Lindenmayer 2007). As a result, simplifying habitats through processes such
as clearing land for agriculture may have negative effects on existing reptile
populations. Conversely, maintaining habitat heterogeneity within the landscape may
help maintain reptile diversity and abundance.
One potential solution to the reptile decline in the wheatbelt region of southwest
Australia is to implement ‘analog forestry’, which aims to find an equilibrium between
preserving biodiversity and maintaining agricultural sustainability (Lefroy et al. 1993).
Achieving analog forestry in an agricultural setting requires the productive revenue
component of the landscape to be developed in a way which associates more closely
to the structure and function of remaining isolated remnants (Lefroy et al. 1993).
Agroforestry systems may have the potential to meet the analog forestry requirements
as they may provide alternative sources of revenue, whilst assisting in slowing or
reversing land degradation by reducing soil salinity, erosion and preserving or
enhancing biodiversity (Hobbs et al. 1993; Lefroy et al. 1993; Lefroy et al. 2005).
Although some reptiles may be able to persist in disturbed habitats in the short term,
continual disturbances may pose a substantial long-term threat (Fischer et al. 2004;
Cunningham et al. 2007). The presence of a reptile species in recently disturbed
habitats can be misleading if their long-term resource and habitat requirements cannot
be met (Saunders et al. 1991). With increasing evidence of reptile decline in disturbed
agricultural areas (Smith et al. 1996; Sarre 1998; Mac Nally & Brown 2001; Brown et al.
2008), reptile species that already exist in low densities and dependent on large tracts
of structurally complex habitats, are more likely to be negatively affected. If the
structural complexity of their habitats continues to decline in the agricultural landscape,
many reptile species dependent on these resources may become much rarer or even
face extinction (Vesk & Mac Nally 2006).
15
One agroforestry system that is gaining popularity is native sandalwood. There are five
endemic species of sandalwood in Australia and of these, the Western Australian
sandalwood (Santalum spicatum) has commercial significance as it produces a grade
of
oil
similar
to
Indian
sandalwood,
S. album
(Tonts
&
Selwood
2003).
Santalum spicatum occurs across a wide range of environmental conditions.
Distributed throughout the southern semiarid and northern arid areas of WA (Byrne et
al. 2003), it is an ideal profitable perennial crop. Sandalwood from S. spicatum has
been exported from WA for over 150 years, with its peak export period in the 1890s.
While exports declined in the 1920s, it regained its appeal in the late 1980s which
resulted in the regulation of sandalwood harvesting and export by the State
Government (Tonts & Selwood 2003). The commercial attraction of growing
sandalwood plantations in agricultural lands could be beneficial as an intermediary step
between natural bushland by providing a secondary habitat for not only reptiles but
other local fauna and flora.
The aim of the present study was to investigate whether sandalwood plantations in the
wheatbelt of southwest Australia assist in the persistence of reptile populations by
providing additional resources such as food and shelter. It was predicted that reptile
assemblages in sandalwood plantations and remnant vegetation would have similar
abundance with lower abundance in paddocks and that these reptile assemblages
would be more diverse than those on paddocks. In addition, food resources for reptiles
(i.e. invertebrates) were also investigated for variation in abundance and diversity
between paddocks, sandalwood plantations and remnant vegetation.
METHODS
Study site and sampling design
The study was restricted to the 300-600 mm rainfall zone of the WA wheatbelt region
as this is the prime area to establish sandalwood plantations. Three locations were
selected in the vicinity of Pingelly (32° 32’S, 117° 05’E), Bokal (33° 26’S, 116° 54’E)
and Monjebup (34° 15’S, 118° 33’E, Figure 6). Nine sampling sites were selected at
each location, consisting of three replicates within three habitat types: paddock,
sandalwood plantation and remnant vegetation.
Paddocks were cleared agricultural land that had been used for sheep grazing and
annual rotational cropping of wheat, barley, rye and canola for several decades. At the
time of sampling these paddocks had been cropped and had residual stubble. The
16
sandalwood plantation sites were all comprised of native host plants and native
S. spicatum. The plantations at Pingelly were 1-2 years old with a single native host
plant Acacia acumminata. Plantations at Bokal and Monjebup were 3-4 years and 2-3
years old respectively with a mix of native host plants (e.g. Acacia, Banksia, Hakea and
Melaleuca). The remnant vegetation sites were located in national parks or undisturbed
natural bush blocks that were approximately 200 ha, as this area was considered to be
optimal for representing the reptile species present in the natural landscape (Short &
Parsons 2004).
Sample collection
Dry pitfall traps have been shown to be the most effective method for trapping reptiles
(Friend et al. 1989; Moseby & Read 2001; Thompson et al. 2005). A combination of dry
and wet pitfall trapping was undertaken at all sampling sites over Feb-Mar 2009, NovDec 2009 and Jan-Feb 2010, representing the active period of reptiles. Dry pitfall traps
were constructed with 20 L PVC buckets with a 28 cm diameter. At each site 1 ha
trapping grids was installed. Trapping grids consisted of three trap lines spaced 50 m
apart. Each trap line consisted of six pit traps inserted flush to the ground at intervals of
20 m. To optimise capture rates and reduce the risk of animals learning to avoid the
obstruction, a Y-shaped drift fence was erected, made of PVC garden fencing that was
30 cm high with 7 m arms (Friend et al. 1989). A total of 405 pitfall traps were set over
the three locations, where trapping occurred monthly in one week rotations at each
location, yielding 29 160 nights of trapping over the three sampling periods. Traps were
checked daily during the early morning to reduce disturbance of the trapping and more
frequently if extreme weather conditions arose to ensure the welfare of trapped
animals.
Reptiles were identified to species level where possible to describe species
assemblages. Permanent mark-recapture techniques were employed using a toe clip
coding scheme to identify individuals and to ascertain population size. Each toe digit
was allocated a number so that each individual reptile species trapped could be given a
unique number code (see Donnelly et al. 1994). Legless lizards and snakes were
recorded but not permanently marked.
17
FIGURE 6: South-western Australia, showing wheatbelt area (brown), location of study
sites (blue), surrounding cities and towns (black) and major roads (yellow). Source: DAFWA
2010 and Google Earth 2014.
Wet pitfall trapping for invertebrates was conducted for one week in November 2009
and one week in January 2010. Five wet pitfall traps were placed in the area of the
1 ha dry pitfall trap grids, four at the corners and one in the centre. The traps were
plastic vials 70 mm in diameter, 150 mm deep and filled with a 70% solution of ethanol
that was replenished daily. Traps were collected at the end of the week and
invertebrate samples identified to order level using a binocular dissecting microscope.
18
Data analysis
Reptile and invertebrate data were combined by sites for a more robust analysis, there
were no reptile recaptures. Differences between the structure of both reptile and
invertebrate assemblages were analysed by permutational multivariate analysis of
variance (PERMANOVA). Analyses were based on a Bray-Curtis similarity matrix, a
square root transformation was performed on reptile data and a log (X+1)
transformation was performed on invertebrate data. Pair-wise post-hoc tests were
performed to gauge differences in levels of the main effects and within interaction
terms if necessary. The tests incorporated two orthogonal fixed factors (location and
habitat) with sites as replicates (based on 9999 permutations). A canonical analysis of
principal coordinates (CAP) was also performed to further aid in the interpretation of
the PERMANOVA results.
Due to the large number of null trapping records, which did not satisfy the assumption
of normality for ANOVA, a two-way univariate permutational ANOVA was used to test
for differences between reptile and invertebrate species richness and abundance
between the three habitats. All analyses were based on a Euclidean distance similarity
matrix; reptile and invertebrate order richness data were untransformed. A square root
transformation was done on reptile abundance data and a log (X+1) transformation
was performed on invertebrate abundance data. Pair-wise post-hoc tests were used to
gauge differences in levels of the main effects, within interaction terms if necessary.
The tests incorporated two orthogonal fixed factors (location and habitat) with sites as
replicates (based on 9999 permutations).
Further testing was conducted using Distance-based Linear Modelling (DistLM) to
assess if there was any relationship between reptile and invertebrate assemblages. For
the DistLM, the Akaike Information Criterion (AIC) was used to choose between the
different combinations of invertebrate variables selected by a BEST analysis to explain
the reptile assemblage. This was based on the Bray-Curtis resemblance measure, a
square root transformation of the reptile data and log(X+1) transformation on
invertebrate data (based on 9999 permutations).
Analyses were performed using the PRIMER-E statistical package (version 6.1.13)
(Clarke & Gorely 2006) with the PERMANOVA+ add-on (version 1.0.3) (Anderson et al.
2008).
19
RESULTS
Reptiles
Reptiles are classified by life guilds according to Wilson & Swan 2008. A total of 552
reptiles from 28 species were trapped across the three locations (Table 1). This
included 175 reptiles (14 species) trapped at Pingelly, 137 reptiles (14 species) at Bokal
and 240 reptiles (17 species) at Monjebup. As no reptiles were recaptured during the
trapping period, population estimates were not obtained.
Multivariate PERMANOVA showed there was a significant effect of both location and
habitat on reptile assemblages but no interaction effect between those two factors
(Table 2). Pair-wise tests for location revealed a significant difference between reptile
assemblages at Monjebup, but not at the locations Pingelly and Bokal (Table 3a). Pairwise tests for habitat showed that reptile assemblages were significantly different in the
remnant habitats but not for paddock and sandalwood habitats (Table 3b).
20
TABLE 1: Mean (± SE) number of reptile species per site caught across the three different habitats (Pad = Paddock, San = Sandalwood, Rem = Remnant) at
each location: Pingelly, Bokal and Monjebup over the active reptile periods Feb-Mar 2009, Nov-Dec 2009 and Jan-Feb 2010. Life guilds: Terrestrial (t),
Fossorial (f), Saxicolous (s) and Arboreal (a).
Scientific name
Common name
Christinus marmoratus
(s, a)
Crenadactylus ocellatus
Underwoodisaurus millii
Southwestern Clawless Gecko
(t, s)
(t)
(t, s)
Aprasia repens
0.17 ± 0.09
Wheatbelt Stone Gecko
0.17 ± 0.09
0.28 ± 0.11
Barking Gecko
0.06 ± 0.06
0.11 ± 0.08
Fraser's Delma
Lialis burtonis
(t)
Burton's Legless Lizard
Pogona minor
(t, a)
(t,s)
(t)
Hemiergis initialis
(t)
Hemiergis peronii
(t)
Lerista distinguenda
(t)
(t)
Liopholis multiscutata
0.11 ± 0.08
Monjebup
San
Rem
0.06 ± 0.06
0.33 ± 0.16
0.06 ± 0.06
0.28 ± 0.16
0.11 ± 0.08
0.06 ± 0.06
0.06 ± 0.06
0.11 ± 0.08
0.17 ± 0.09
0.22 ± 0.17
Callose-palmed Fence Skink
Broad-banded Sandswimmer
(t, s)
(t, s)
(t, s)
(t)
0.11 ± 0.08
0.61 ± 0.20
0.44 ± 0.18
0.06 ± 0.06
0.06 ± 0.06
0.06 ± 0.06
0.50 ± 0.15
0.06 ± 0.06
0.11 ± 0.08
Ramphotyphlops australis
Ramphotyphlops waitii
(t)
0.11 ± 0.08
0.11 ± 0.08
0.28 ± 0.14
Four-toed Mulch Skink
2.00 ± 0.97
1.17 ± 0.32
1.39 ± 0.29
0.06 ± 0.06
Common Dwarf Skink
2.83 ± 1.32
Woodland Dark-flecked Morethia
0.06 ± 0.06
0.28 ± 0.18
0.06 ± 0.06
0.33 ± 0.14
0.44 ± 0.34
0.72 ± 0.21
0.06 ± 0.06
2.56 ± 1.41
1.61 ± 0.75
0.39 ± 0.61
West Coast Pale-flecked Morethia
0.11 ± 0.08
Shrubland Pale-flecked Morethia
1.22 ± 0.48
Southwestern Blind Snake
(f)
Parasuta nigriceps
Pseudonaja affinis
(t)
Simoselaps bertholdi
(t)
0.33 ± 0.14
1.39 ± 0.62
0.67 ± 0.44
1.06 ± 0.33
0.11 ± 0.08
0.11 ± 0.08
0.67 ± 0.24
1.61 ± 0.44
0.06 ± 0.06
0.06 ± 0.06
0.06 ± 0.06
0.06 ± 0.06
0.17 ± 0.17
0.06 ± 0.06
0.11 ± 0.08
0.28 ± 0.11
0.11 ± 0.08
0.06 ± 0.06
0.33 ± 0.14
0.06 ± 0.06
0.44 ± 0.23
0.33 ± 0.11
0.22 ± 0.13
0.06 ± 0.06
0.06 ± 0.06
Gould's Hooded Snake
(t)
0.83 ± 0.34
Southern Five-toed Mulch Skink
Western Bobtail / Shingleback
(f)
0.06 ± 0.06
0.28 ± 0.14
0.06 ± 0.06
Bull-headed Skink
(t)
Parasuta gouldii
Pad
0.06 ± 0.06
Southwestern Cool Skink
(a)
Southwestern Four-toed Lerista
(t)
Morethia lineoocellata
Tiliqua rugosa
Rem
Odd-striped Ctenotus
Eremiascincus richardsonii
Morethia obscura
Bokal
San
0.11 ± 0.08
Gould's Sand Monitor
Cryptoblepharus plagiocephalus
Morethia butleri
0.06 ± 0.06
Western Bearded Dragon
(t)
Acritoscincus trilineatum
Menetia greyii
Pad
Southwestern Sandplain Worm Lizard
Delma fraseri
Ctenotus impar
Rem
0.11 ± 0.11
(t)
Varanus gouldii
Pingelly
San
Western Marbled Gecko
(t, s)
Diplodactylus granariensis
Pad
0.06 ± 0.06
Black-backed Hooded Snake
0.06 ± 0.06
Dugite
0.06 ± 0.06
Jan's Banded Snake
0.06 ± 0.06
0.17 ± 0.09
0.06 ± 0.06
21
TABLE 2: Permutational multivariate analysis of variance based on Bray-Curtis
similarities testing the effect of location and habitat on reptile assemblage structure.
P≤0.05*, P≤0.0001***.
Number of
Mean
Source of variation
unique
d.f.
Squares
Pseudo-F
P(perm)
permutations
Location
2
4517
3.1688
0.0018*
9934
Habitat
2
9014
6.3233
0.0001***
9908
Location x Habitat
4
1565
1.0978
0.3645
9903
Residuals
17
1426
Total
25
TABLE 3: Pair-wise post-hoc analysis of reptile assemblages based on Bray-Curtis
similarities (a) between locations and (b) between habitats. P = Pingelly, B = Bokal,
M = Monjebup. Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*,
P≤0.001**.
(a)
Location
t
P,B
1.3771
P,M
B,M
P(perm)
(b)
Habitat
t
P(perm)
0.1073
Pad, San
1.2087
0.2192
2.9554
0.0002**
Pad, Rem
2.6315
0.0007**
2.9802
0.0002**
San, Rem
1.5153
0.0392*
CAP ordination clearly indicated that the reptile assemblages at Monjebup were
different from those at Pingelly and Bokal (Figure 7). As Monjebup is the most southern
location, a change in reptile assemblages is to be expected. The main cause for this
would be the presence of Hemiergis peronii and H. initialis, skinks associated with
wetter, cooler climates, which were only found at Monjebup.
CAP also illustrates a gradient of change in reptile assemblage structure from paddock
to sandalwood to remnant. Reptile abundance was high in the remnant vegetation with
the exception of Mentia greyii and H. peronii which had higher numbers in the paddock
and similar numbers in the sandalwood plantation and remnant vegetation. While some
reptile species were restricted to only the remnant vegetation (Aprasia repens,
Christinus marmoratus, Ctenotus impar, Liopholis multiscutata, Lialis burtonis,
Tiliqua rugosa, Parasuta gouldii and Parasuta nigriceps) the majority of the reptile
assemblage were present in remnant vegetation and sandalwood plantation but rarely
in paddock (with the exception of Ramphotyphlops australis which was found mainly in
paddocks and remnant vegetation).
22
Legend
0.4
Pad - Pingelly
San- Pingelly
Rem- Pingelly
Pad - Bokal
San- Bokal
Rem- Bokal
Pad - Monjebup
San- Monjebup
Rem- Monjebup
0.2
CAP 2
R. australis
0
H. peronii
H. initialis
S. bertholdi
U. millii
D. granariensis
L. multiscutata
-0.2
C. plagioecphalus
M.obscura
-0.4
-0.4
-0.2
0
0.2
0.4
CAP1
FIGURE 7: CAP ordination plot relating reptiles to habitat: paddock (Pad), sandalwood
(San) and remnant (Rem) and location (based on Bray Curtis after square root
transformation, vector overlay of dominant reptile species habitat association based on
Spearman’s correlation >0.6).
Two-way univariate tests showed no significant effect of habitat (P=0.1633) or location
(P=0.1618) on reptile abundance and there was no interaction effect. There was a
significant effect of habitat (P= 0.0024) on reptile species richness but not location
(P=0.2286), there was no interaction effects. Analysis revealed reptile species richness
was higher in the remnant followed by sandalwood and then paddock (Table 4a).
Reptile species richness was significantly different between the remnant and paddock
and remnant and sandalwood (Table 4b).
23
TABLE 4: (a) Mean (± SE) reptile abundance and species richness (number of habitat
per site). Numbers were summed across three sites in each habitat at each location
and averaged across location for each habitat. (b) Univariate pair-wise post-hoc
analysis of reptile species richness based on Euclidean distance between habitats.
Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*.
(a)
Habitat
Abundance (N)
Richness (S)
Paddock
4.51 ± 0.63
3.5 ± 0.42
Sandalwood
3.63 ± 0.34
4.89 ± 0.59
Remnant
4.93 ± 0.52
8.44 ± 1.094
(b)
Reptile Species Richness (S)
Habitat
t
P(perm)
Pad, San
1.801
0.1044
Pad, Rem
3.788
0.0045*
San, Rem
2.705
0.0226*
Invertebrates
A total of 17 invertebrate orders were captured across the three locations during the
one week trapping periods in November 2009 and January 2010 (Table 5). Multivariate
PERMANOVA showed there was a significant effect of location and habitat on
invertebrate assemblages. There were no interaction effects between the two factors
(Table 6).
Pair-wise tests for location revealed a significant difference between invertebrate
assemblages at Monjebup but not at Pingely and Bokal (Table 7a). Pair-wise tests for
habitat showed that assemblages were significantly different amongst all three habitats
(i.e. paddock and sandalwood habitats, paddock and remnant habitats and sandalwood
and remnant habitats; Table 7b).
24
TABLE 5: Mean (± SE) number of invertebrates per site, grouped by order, trapped over a one week period in the months November 2009 and
January 2010. The order Hymenoptera was separated into ants and wasps and bees. Pad = Paddock, San = Sandalwood, Rem = Remnant.
Pingelly
Order
Araneae
Bokal
Monjebup
Pad
San
Rem
Pad
San
Rem
Pad
San
Rem
9 ±6
18 ± 7
16 ± 3
12 ± 1
15 ± 2
12 ± 1
26 ± 4
22 ± 5
12 ± 1
1±1
5±3
6±7
9±9
5±2
Acarina
3±2
Scorpionida
Chilopoda
0.3 ± 1
1±1
1±1
1±1
1±1
0.3 ± 1
3±1
1 ± 0.4
0.3 ± 1
1±1
Diplopoda
0.3 ± 1
Thysanura
1±2
Blattodea
Isoptera
2±1
2±1
3±5
Dermaptera
0.3 ± 1
1±1
1±2
1±1
0.3 ± 1
2±1
1±2
1±1
2±2
1±1
0.3 ± 1
73 ± 73
3±2
33 ± 20
116 ± 66
16 ± 11
Orthoptera
2±1
1±2
5±3
4 ± 0.3
9±5
3±1
44 ± 31
19 ± 3
19 ± 7
Hemiptera
15 ± 15
11 ± 6
4±1
6±4
13 ± 4
2±2
13 ± 7
9±1
6±1
Coleoptera
23 ± 14
187 ± 128
56 ± 32
56 ± 40
37 ± 4
24 ± 161
54 ± 25
45 ± 18
29 ± 14
Diptera
11 ± 7
15 ± 1
9±3
12 ± 2
19 ± 5
18 ± 7
104 ± 63
45 ± 10
40 ± 10
Lepidoptera
1±1
1±0
0.3 ± 1
0.3 ± 1
2±1
1±1
2±1
2 ± 0.3
Thysanoptera
Hymenoptera (wasp/bee)
Hymenoptera (ant)
Isopoda
25
25
6±4
1±2
1±2
3±2
19 ± 4
24 ± 8
9±4
15 ± 3
16 ± 6
19 ± 7
15 ± 5
11 ± 1
735 ± 619
1474 ± 201
1907 ± 652
365 ± 160
932 ± 221
1143 ± 241
662 ± 405
1941 ± 479
1574 ± 556
0.3 ± 1
0.3 ± 1
1±2
0.3 ± 1
0.3 ± 1
7 ± 12
TABLE 6: Permutational multivariate analysis of variance based on Bray-Curtis
similarities testing the effect of location and habitat on invertebrate assemblage
structure. P≤0.001**.
Number of
Mean
Source of variation
unique
d.f.
Squares
Pseudo-F
P(perm)
permutations
Location
2
562
2.9652
0.0003**
9917
Habitat
2
863
4.556
0.0002**
9929
Location x Habitat
4
145
0.7647
0.8113
9891
Residuals
17
189
Total
25
TABLE 7: Pair-wise post-hoc analysis of invertebrate assemblages based on Bray-Curtis
similarities (a) between locations and (b) between habitats. P = Pingelly, B = Bokal,
M = Monjebup. Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*,
P≤0.001**
(a)
Location
t
P,B
1.1884
P,M
B,M
P(perm)
(b)
Habitat
t
P(perm)
0.2166
Pad, San
1.5694
0.0236*
2.5484
0.0005**
Pad, Rem 1.782
0.0046*
2.433
0.0007**
San, Rem 1.7768
0.0069*
At Bokal and Pingelly CAP ordination indicated a difference in invertebrate
assemblages in the paddock with overlap between the sandalwood and remnant
assemblages (Figure 8). However, Monjebup invertebrate assemblages were similar
across the three habitats. This could be due to paddock sites in Monjebup all having
been planted during the sampling period, whereas at Pingelly and Bokal there was a
mixture of planted and fallow paddocks.
26
Legend
0.6
Pad - Pingelly
San- Pingelly
Rem- Pingelly
Pad - Bokal
San- Bokal
Rem- Bokal
Pad - Monjebup
San- Monjebup
Rem- Monjebup
0.4
0.2
CAP 2
Diptera
Orthoptera
Dermaptera
0
Acarina
-0.2
Thysanura
Hymenoptera (Other)
-0.4
-0.4
-0.2
0
0.2
0.4
CAP1
FIGURE 8: CAP ordination plot relating invertebrates to habitat: paddock (Pad),
sandalwood (San) and remnant (Rem) and location (based on Bray Curtis after
Log(X+1) transformation, vector overlay of dominant invertebrate orders habitat
association based on Spearman’s correlation >0.6).
Two-way univariate tests showed a significant effect of location and habitat on
invertebrate abundance (P= 0.0265, P= 0.0552 respectively) and invertebrate order
richness (P= 0.0094, P= 0.0329 respectively) with no interaction effects. Invertebrate
abundance and order richness were both lower in paddock habitats and similar
between remnant vegetation and sandalwood plantation (Table 8a). Invertebrate
abundance was lower at Bokal but similar between Pingelly and Monjebup. However,
invertebrate order richness was higher at Monjebup and similar between Pingelly and
Bokal (Table 8b).
27
TABLE 8: (a) Mean (± SE) invertebrate abundance and invertebrate order richness
(number of habitat per site). Numbers were summed across three sites in each habitat
at each location and averaged across location for each habitat. (b) Univariate pair-wise
post-hoc analysis of invertebrate abundance and order richness based on Euclidean
distance between locations and between habitats. P = Pingelly, B =
Bokal, M =
Monjebup. Pad = Paddock, San = Sandalwood, Rem = Remnant. P≤0.05*.
(a)
Location
Abundance (N)
Order Richness (S)
Pingelly
7.33 ± 0.19
8.50 ± 0.42
Bokal
6.66 ± 0.25
8.44 ± 0.56
Monjebup
7.25 ± 0.20
9.89 ± 0.46
Abundance (N)
Order Richness (S)
Paddock
6.51 ± 0.27
7.9 ± 0.48
Sandalwood
7.34 ± 0.15
8.9 ± 0.35
Remnant
7.30 ± 0.53
10 ± 0.50
Habitat
(b)
Abundance (N)
Location
t
P,B
2.2312
P,M
B,M
P(perm)
Order Richness (S)
t
P(perm)
0.0418*
0.0099
0.9234
0.1587
0.872
2.4962
0.0345*
2.2189
0.0479*
2.414
0.0327*
Abundance (N)
P(perm)
Order Richness (S)
Habitat
t
t
P(perm)
Pad, San
2.8382
0.0176*
2.2754
0.0432*
Pad, Rem
2.3486
0.04*
3.1344
0.0095*
San, Rem
0.19403
0.8495
1.8898
0.0919
DistLM analysis was originally run on all data, however results showed a bias towards
locations and hence Monjebup data were omitted and the analysis re-run on Pingellly
and Bokal data. The DistLM established that 93% of the variation in the reptile
assemblage was attributed to 15 measured invertebrate orders (Figure 9). This
suggests that invertebrates can be used to predict reptile assemblage with 93%
certainty. The DistLM showed out of the 15 invertebrate orders, the best fit to predict
reptile assemblages are Acarina (18%), Hymenoptera (not ants, 16%) and Hemiptera
(11%).
28
Legend
dbRDA2 (23.1% of fitted, 21.5% of total variation)
40
Pad - Pingelly
San - Pingelly
Rem - Pingellly
Pad - Bokal
San - Bokal
Rem - Bokal
20
Hemiptera
Hymenoptera (Other)
Acarina
0
-20
-40
-60
-40
-20
0
20
40
dbRDA1 (32.8% of fitted, 30.6% of total variation)
FIGURE 9: DistLM plot for reptile data using the ‘BEST’ selection procedure on the
bases of the AIC selection criterion (based on Bray Curtis after square root
transformation), overlaid with invertebrate data. Pad = Paddock, San = Sandalwood,
Rem = Remnant.
Result summary
A comparison of reptile and invertebrate abundance, richness and assemblages across
habitats is summarised in Table 9. Reptile abundance was similar amongst all three
habitats, whereas invertebrate abundance was higher in remnant vegetation compared
to paddock and similar in remnant vegetation and sandalwood plantation. Invertebrate
abundance was greater in sandalwood plantation habitat than paddock habitat. Reptile
species richness and invertebrate order richness had the same trend where it was
highest in remnant vegetation followed by sandalwood plantation and then paddock.
Reptile assemblages were different in remnant vegetation but were similar between
paddock and sandalwood plantations. Invertebrate assemblages were different
amongst all three habitats.
29
TABLE 9: Result summary of reptile and invertebrate abundance, richness and
assemblages.
Pad = Paddock,
San =
Sandalwood,
Rem = Remnant.
P≤0.05*,
P≤0.001**.
Pad vs San
Pad vs Rem
San vs Rem
Reptile abundance
Pad = San
Pad = Rem
San = Rem
Invertebrate abundance
Pad < San*
Pad < Rem*
San = Rem
Reptile species richness
Pad = San
Pad < Rem*
San < Rem*
Invertebrate order richness
Pad < San*
Pad < Rem*
San = Rem
Reptile assemblages
Pad = San
Pad ≠ Rem
San ≠ Rem
Invertebrate assemblages
Pad ≠ San
Pad ≠ Rem
Pad ≠ Rem
DISCUSSION
Contrary to expectations, reptile assemblages did not have similar abundance in
sandalwood plantations and remnant vegetation with lower abundance in paddocks.
Rather, it was found that reptiles had similar abundance across all three habitats. In
contrast, invertebrate assemblages had similar abundances in sandalwood and
remnant vegetation habitats, where both sandalwood and remnant were higher in
abundance compared to paddock habitats. While reptile and invertebrate abundances
showed different trends, both reptile species richness and invertebrate order richness
met expectations where they would be higher in the remnant vegetation followed by the
sandalwood plantation and then paddock. However, reptile species richness did not
differ between sandalwood plantations and paddock habitats.
These findings suggest reptile assemblages may be slower to recover than
invertebrate assemblages on revegetated agricultural land. Invertebrate assemblages
had lower abundance and diversity in the paddock and slightly higher diversity in the
remnant vegetation than the sandalwood plantation. CAP ordination (Figure 8) shows
invertebrate assemblages to be much closer to those in remnant vegetation than
paddocks in the study locations Pingelly and Bokal. Results suggest invertebrate
assemblages in sandalwood plantations may be reverting towards assemblages found
in remnant vegetation. Haddad et al. (2001) found a direct link between the diversity of
invertebrates and plant diversity, plant functional group diversity and plant structural
variety. Using a variety of native mix host plants in the sandalwood plantation increases
structural heterogeneity within the sandalwood plantation. This encourages a greater
range of invertebrates to recolonise and increase invertebrate diversity in these areas.
30
Of the invertebrates caught in this study, the most abundant were from the order
Hymenoptera. Invertebrates from this order are renowned for their diversity as
predators, parasitoids and pollinators (Austin et al. 2004). In an agroforestry and
agricultural system, Hymenoptera are seen as beneficial insects that help regulate the
density of pest insect populations and assist in flora reproduction (Queiroz et al. 2006).
Hymenoptera in this study favoured the remnant vegetation and sandalwood
plantation. From a land management perspective, it is desirable to retain these
beneficial insects within the landscape. Santos et al. (2007) and Auad et al. (2012)
found that vegetative structural heterogeneity promoted higher richness and diversity of
predatory wasp species. The complex environment created through vegetative
structural diversity provided more microhabitats, better protection from predators, and
increased availability and diversity of food resources and nesting substrates.
Although young sandalwood plantations (<10 years) are not as effective as remnant
vegetation in providing alternative habitat resources for reptiles, these plantations do
seem to offer an extended resource for invertebrates, which is the main food source for
reptiles. In an 11 year study, Haddad et al. (2011) found that higher plant diversity
stabilised invertebrate assemblages across trophic levels. The study found that higher
plant diversity stabilised the herbaceous and predatory invertebrate richness while also
increasing invertebrate herbivore abundance. Haddad et al. (2011) suggested that
increasing plant diversity provides a more reliable food and habitat resource for
invertebrates. Therefore, by establishing native mix host sandalwood plantations, it
may provide effective benefits for increasing fauna diversity. As these sandalwood
plantations mature, they could have the potential to provide future habitat resources for
reptiles and encourage re-colonisation.
While sandalwood plantations supported a larger more diverse assemblage of
invertebrates than paddocks, this was not the case for reptiles. This study found that
reptile abundance was similar across the three habitats. Reptile assemblages in
sandalwood plantations were similar to paddocks compared to remnant vegetation.
This may be due to the plantations being relatively young (1-3 years). The immaturity of
the plantations may not be providing enough varied habitat resources for reptiles to
recolonise. Hobbs et al. (2003a) suggested that while plantations offer more habitat
structure in terms of tree stems and canopy cover compared with annual pastures,
there is still a lack of ground layer in plantations. Vesk and Mac Nally (2006) and Vesk
et al. (2008) also suggested that mature and senescing vegetation are critical habitat
requirements for fauna to utilise as ecological resources, for activities such as foraging,
reproduction and nesting. Previous studies have shown that different reptile species
31
require different habitats, and as a result, species diversity increases as variation in
structural habitat increases (Fischer et al. 2004; Cunningham et al. 2007; Mott et al.
2010). In addition, some plantation management practices such as high density
plantings, removal of wood/rock debris and vegetation clearing to prevent fire
outbreaks may retard the development of habitats that promote the return of reptile
assemblages back into revegetated land. These management practices reduce the
amount of large spreading canopy cover, fallen timber, tree hollows and diverse ground
vegetation which form the required habitat that promotes and maintains species
diversity (Vesk et al. 2008). Vesk et al. (2008) suggested management practices
should incorporate low-density heterogeneous plantings whilst integrating spatial
variation and retaining dead trees and logs. By doing so, it will reduce the time required
to develop structural habitat diversity. A recent study by Michael et al. (2011) also
highlighted the importance of retaining rocky habitats in the landscape as they support
reptile species. These rocky habitats are often associated with characteristics of old
growth vegetation such as exfoliating bark, dead trees and fallen timber.
Maintaining structural habitat diversity in the landscape is important for encouraging
reptile re-colonisation. Reptiles can be grouped into three main life guilds: terrestrial,
fossorial and scansorial (i.e. saxicolous or arboreal). How reptiles utilise available
habitat resources determine which life guilds they are grouped in. The reptiles caught
in this study were primarily terrestrial and/or fossorial species with the exception of
Christinus marmoratus, a saxicolous and semi-arboreal gecko, Cryptoblepharus
plagiocephalus an arboreal skink and Pogona minor a semi-arboreal dragon. Michael
et al. (2011) found that terrestrial and fossorial species had a positive response to
forest regrowth and land revegetation. This could explain the change in reptile
assemblages across the three habitats in this study (see Figure 7). Observations
during this study found that saxicolous and arboreal species were mostly restricted to
the remnant vegetation, in favour for plant structural diversity. Terrestrial and fossorial
species were interchanging between the remnant vegetation and sandalwood
plantation as both habitats had greater leaf litter depth and cover than paddock
habitats. However, due to low numbers caught during this study at each location,
further investigation is required to confirm this.
All reptile species trapped in this study had higher numbers in the remnant vegetation
with the exception of two generalist skinks Hemiergis peronii and Mentia greyii, which
had greater numbers in the paddock and similar numbers in the sandalwood plantation
and remnant vegetation. According to Brown et al. (2011), an increase in abundance in
small generalist skinks in paddocks may be explained by their preferences for bare
32
ground and increased light exposure. Craig et al. (2010) also found this to be true in his
vegetative rehabilitation study where two small generalist skinks, were more abundant
in thinned and burned sites. Generalist reptile species have less specific habitat
requirements than specialist reptile species and therefore can adapt to a wider range of
environmental conditions. This adaptability has increased their ability to disperse
between remnant vegetation by existing in sub-optimal habitats and agricultural lands
(Smith et al. 1996).
The majority of reptile species caught in this study were generalists that actively hunt
for their prey. The exceptions were two legless lizards (Aprasia repens and
Lialis burtonis) which are diurnal and two blind snakes (Ramphotyphlops australis and
R. waitii) which are nocturnal. Aprasia repens, R. australis and R. waitii specialise in
eating ant larvae, while L. burtonis specialises in hunting skinks and Tiliqua rugosa
which are omnivorous (Wilson & Swan 2008). These reptile specialists were found
mainly restricted to the remnant vegetation and sandalwood plantation with native
mixed host plants. This highlights the importance of retaining vegetative structural
diversity in order to encourage and maintain species diversity.
One of the major limitations of managing reptile populations is the limited knowledge of
their ecology. There is a need for long-term monitoring of reptile populations to fill this
gap. The results of this study suggest that perennial plantings and old-growth
woodlands are not readily interchangeable habitats. As perennial plantings mature,
they may provide an alternative means of maintaining reptile biodiversity in agricultural
lands. While young sandalwood plantations (<10 years) do not provide the same
structure and diversity of habitat resources as remnant vegetation, they are more likely
to provide better habitat resources than agricultural paddocks, especially as they
mature. However, there is still a need for regular monitoring of reptile populations in
agroforestry plantations as they mature and after harvesting to test the ecological value
of these habitats in the long-term (see Lindenmayer et al. 2012).
The continual preservation and improvement of vegetation heterogeneity in agricultural
landscapes is likely to contribute to maintaining higher diversity of invertebrate and
reptile assemblages. Furthermore, sandalwood plantations that utilises a variety of
mixed native host plants may be better at providing more habitat resources than
sandalwood plantations with mono-host plants and homogenous plantations (e.g. oil
mallee, pine and blue gum). However, to confirm this, further investigation at a
functional group level would be needed to gain a better understanding of the ecological
33
roles invertebrates and reptiles play in a sandalwood plantation; this is investigated in
Chapter 3.
34
CHAPTER 3
REPTILE TROPHIC STRUCTURE IN
SANDALWOOD AGROFORESTRY
Menetia greyii a four finger, five toe generalist skink.
TROPHIC RELATIONSHIPS OF MENETIA GREYII IN SANDALWOOD
PLANTATIONS COMPARED TO NATIVE AND CROPPED ECOSYSTEMS IN
SOUTHWEST AUSTRALIA
ABSTRACT
This study used the stable isotopes δ13C and δ15N to examine trophic relationships of
Menetia greyii within a sandalwood agroforestry landscape. The aim was to determine
if trophic structure differed among three habitats (paddock, sandalwood plantation and
remnant vegetation) and to gauge if food web complexity in sandalwood plantations
was greater than in cropped systems and simpler when compared to more complex
habitats like natural vegetation. I collected tissue samples of M. greyii as well as of
foliage from the dominant vegetation sources and invertebrates representing the three
feeding guilds (herbivores, carnivores and omnivores) at three sites in southwest
Australia. Source (primary production) δ13C was within the normal range of C3 plants
and as there was no δ13C and δ15N interaction, only the δ15N values were analysed.
Across the three habitats, δ15N of vegetation (primary producers) were most enriched
in the sandalwood plantation (-0.01 ‰ to 0.5 ‰) and slightly depleted in remnant
vegetation (-2.1 ‰ to 0.7 ‰). Consumer δ15N values for invertebrates were between
5.6 ‰ to 8.3 ‰ and δ15N values for M. greyii were more enriched (6 ‰ to 8.5 ‰).
Whilst there was no difference in the trophic position of M. greyii amongst the three
habitats, M. greyii in paddock and sandalwood plantation habitats exhibited an
omnivorous diet compared to remnant vegetation habitat where they exhibited a more
carnivorous diet. This suggests the generalist diet of M. greyii allows it to successfully
adjust to modified rural landscape changes.
INTRODUCTION
The intensification of land clearing and loss of perennial vegetation though farming
practices in agricultural landscapes has vastly modified habitats for many species in
southwest Australia (Hobbs et al. 1993). Modified landscapes can put more pressure
on declining species, resulting in a change in their biology, behaviour and species
interactions; these changes in turn can also affect breeding patterns and social
systems (Fischer & Lindenmayer 2007). However, over recent decades there has been
significant re-establishment of perennial vegetation in southwest Australia in the form of
agroforestry plantations, which has the potential to enhance biodiversity and restore
habitats in agricultural landscapes, particularly in the medium to lower rainfall
agricultural zones (McKinnell et al. 2008). However, the potential of these agroforestry
36
plantations to elevate biological pressures of declining species in these modified lands
has not been well described (Roberge et al. 2013).
Reptiles are particularly sensitive to land use changes, especially in agricultural lands
(Sarre et al. 1995; Smith et al. 1996; Sarre 1998; Mac Nally & Brown 2001; Driscoll
2004). Most reptiles have a low dispersal ability (Fischer et al. 2003; Driscoll 2004;
Fischer et al. 2004), which means that changes in habitat connectivity and shifts in
plant species dominance may have a major impact on reptile habitat and food
requirements, such as invertebrate populations. A majority of reptile species, including
lizards, reside and forage in the ground-layer, litter or subsoil. These areas are also
more likely to be subjected to degradation through agricultural practices through
processes such as overgrazing, soil compaction, weed invasion and removal of woody
debris (Brown 2001). Most reptiles are opportunistic insectivorous feeders, foraging
through active search or sit-and-wait behaviours (Pianka 1973). Consequently,
studying insects and their responses to modified or restored landscapes can lead to a
better understanding of their trophic links to reptiles. Understanding any shift in trophic
position of reptiles can provide an indication of the responses of trophically similar
species to modified habitats.
Trophic structure forms the basis of food webs, which can be traced though trophic
links, these links provide a way to analyse overall assemblages of direct and indirect
effects of environmental stress and disturbance (De Ruiter et al. 2005). Trophic links
provide network stability and is often linked to connective distributions within network
topology that can be assessed by measuring the distribution of links among species
(Thomas et al. 2009). The connections determine the flow of energy from one species
to another and the full topology of the network determines the fragility and stability of
these systems (Allesina et al. 2009). On average, species within food webs are
typically separated by less than three links (De Ruiter et al. 1995; Dunne et al. 2002;
Williams et al. 2002; Montoya et al. 2006). Disturbance effects on one species can
affect other species that are linked via the shortest path in a food web (Paine 1966;
Thomas et al. 2009). Such ‘short circuits’ suggest biological disturbances may spread
faster than initially expected in complex food webs (De Ruiter et al. 1995; Montoya et
al. 2006). In modified landscapes, the likelihood of such ‘short circuits’ is high and the
resulting imbalance in trophic structure is a concern.
Food web interactions have been assessed using stable isotopes to directly trace the
cycling of elements (Fry 2006). In particular, δ13C and δ15N can be used to determine
the trophic interactions between a wide variety of species within food webs (Peterson &
37
Fry 1987). The C stable isotope composition of organic matter, denoted as δ13C, has
been used previously to estimate dietary sources, identify movement and to establish
the baseline for estimation of trophic levels across a range of ecosystems (Peterson &
Fry 1987; Hobson 1999; O'Reilly et al. 2002; Post 2002). In contrast, the N stable
isotope composition of organic matter, denoted as δ15N, is often used to estimate
trophic position owing to the accumulation of the heavier isotope in the diet of a
consumer and its enrichment by 3-4‰ in successive links in food webs (Peterson & Fry
1987; O'Reilly et al. 2002; Layman et al. 2007). Stable isotope analysis can also provide
insight as to how individuals or guilds may shift feeding strategies under different
management regimes (Fry 2006). For example, Gibb & Cunningham (2011) showed
that ant communities in revegetated land had a herbaceous diet and fed lower in the
food web, hence simplifying the food web in revegetated land.
The Common dwarf skink (Menetia greyii) is one of the most widespread skink species
in Australia (Adams et al. 2003; Pianka 2011). This makes it an ideal species for
examining shifts in feeding behaviour in modified or restored landscapes. Menetia
greyii are small insectivorous reptiles with an average snout vent length of 40 mm. It
was once believed that M. greyii were an opportunistic insectivorous skink that fed on a
variety of small invertebrates such as termites, bugs, ants, beetles, spiders, moths,
flies, small cockroaches, pseudoscorpions and grasshopper nymphs (Smyth & Smith
1974). However, Pianka (2011) recently found that while M. greyii appeared to be
somewhat opportunistic feeders, their diet is more restricted to silverfish, small spiders,
and true bugs. Menetia species are cryptozoic and are found in a range of habitats
throughout mainland Australia (Gardener et al. 2004). While there may be a variety of
prey items available to M. greyii under natural conditions, loss of habitat, land
degradation and changes to food sources can cause complex biological disturbances.
Whilst the effects of disturbance to trophic structure on M. greyii are unknown, some
sort of trophic shift between modified, restored and natural landscapes would be
expected.
Here, I focused on M. greyii, to investigate how fauna respond to short-term
management programs. This approach is also useful for assessing their response to
longer-term selection forces such as population and species evolution (Fry 2006).
There are numerous stable isotope studies on aquatic food webs (e.g. Fantle et al.
1999; Carabel et al. 2009; Coat et al. 2009; Dekar et al. 2009; Botto et al. 2011) and on
feeding habits of large terrestrial vertebrates, birds, and insects (e.g. Hobson 1999;
Struck et al. 2002; Rubenstein & Hobson 2004; Kupfer et al. 2006; Kerry et al. 2008).
However, there are very few studies using stable isotopes to investigate how
38
vertebrates interact with other trophic levels in modified agro-ecosystems. Here I
investigate the trophic relationships of M. greyii within a sandalwood (Santalum
spicatum) agroforestry landscape to assess whether these differed to those in
surrounding land uses.
Sandalwood is planted as a commercial crop in southwest Australia. If sandalwood
plantations are indeed suitable habitat for M. greyii, it would be expected that food web
complexity in sandalwood plantations will be greater than cropped systems and simpler
when compared to more complex habitats like natural vegetation. I compared the
trophic structure of sandalwood plantations to adjacent paddock cleared of all perennial
vegetation and remnant native vegetation in order to determine if there are any trophic
level effects between the three different habitats.
METHODS
Study site and sampling design
Three locations, at least 140-246 km apart, were selected in the vicinity of Pingelly
(32° 32’S, 117° 05’E), Bokal (33° 26’S, 116° 54’E) and Monjebup (34° 15’S, 118° 33’E;
see Figure 6, Chapter 2). All sites were within the 300-600 mm rainfall zone of the
wheatbelt area of southern WA. Field sampling occurred over two austral summer
periods: February 2009-March 2009 and November 2009-February 2010. During the
trapping period, Pingelly had average temperatures of 31°C max, 12°C min and total
rainfall of 46 mm, Bokal had average temperatures of 29°C max, 9°C min and total
rainfall of 122 mm and Monjebup had average temperatures of 28°C max, 10°C min
and total rainfall of 105 mm.
At each location, there were nine sampling sites, consisting of three replicates of each
of three habitats: paddock, sandalwood plantation and remnant native vegetation.
Paddocks were agricultural land that had been cleared for several decades and used
for annual rotational cropping of wheat, barley, rye and canola as well as sheep
grazing. At the time of sampling these paddocks had been cropped and had residual
wheat or rye stubble. The sandalwood plantation sites all comprised of native Western
Australian sandalwood, S. spicatum, and associated host plants. Sandalwood is a root
hemiparasitic plant with a wide host range (Hettiarachchi et al. 2010). Previous studies
have used natural abundance stable isotope-mixing models to show that hemiparasitic
plants can access up to 35% of their host's non-structural carbon (Tennakoon & Pate
1996) meaning that their δ13C values will likely reflect that of associated vegetation.
39
All sandalwood plantations were established on land previously used for sheep grazing
and cropping. The plantations at Pingelly were 1-2 years old with a single native host
plant, Acacia accuminata. Plantations at Bokal were 3-4 years old and plantations at
Monjebup were 2-3 years old. Host plants at Bokal and Monjebup were a mix of native
species (e.g. Acacia, Banksia, Hakea and Melaleuca). The remnant native vegetation
sites, which were either in National Park or undisturbed natural bush blocks, had a
minimum area of 200 ha. Habitat extent of 200 ha is considered to be optimal for
representing the reptile species present in the natural landscape (Short & Parsons
2004).
Collection of plant, invertebrate and M. greyii samples
Three replicate samples were taken of the most abundant plant species and consumers
in each of the three habitats at each study location for stable isotope testing. Plant
samples consisted of leaves and leaf litter as they are the primary food source for
herbaceous and detritivorous invertebrates, which make up the majority of M. greyii’s
diet (Smyth & Smith 1974). A total of 131 plant samples (57 woody, 52 herbaceous and
22 leaf litter) were collected from the three habitats. Samples included 36 at the
sandalwood sites, 31 from the pasture sites and 64 from the remnant vegetation
(see Appendix I).
A total of 118 invertebrates (37 herbivores, 32 carnivores and 49 omnivores) were
collected and 53 samples from M.greyii individuals from the three habitats at each of
the 27 sampling sites across the three study locations. Dry pitfall trapping was used to
collect primary and secondary consumers (herbaceous invertebrates that feed on the
vegetation within the three habitats, non-herbaceous invertebrates and M. greyii). Each
sampling site had 1 ha trapping grids made up of three lines of five dry pitfall traps
within the 27 sampling sites. Dry pitfall traps consisted of 20 L PVC buckets with a
diameter of 28 cm. Dry pitfall traps were inserted flush to the ground, 20 m apart along
each line. Each dry pitfall trap had three 30 cm high, PVC garden fencing drift fences
erected in an Y-shaped formation. Each fence was 7 m in length as this is considered
to be the most effective method for trapping reptiles (Friend et al. 1989; Moseby &
Read 2001; Thompson et al. 2005).
Traps were checked daily for M. greyii and other vertebrate species during the early
morning and more frequently if extreme weather conditions arose (i.e. above 40°C and
below 0°C). Tail clippings of M. greyii were collected for stable isotope analyses.
Samples of terrestrial invertebrates for stable isotope analyses were captured via dry
pitfall traps and opportunistically hand collected. Invertebrates were euthanized through
40
chilling and later identified to genus (where possible) and then grouped as herbivores,
carnivores and omnivores based on species identification, examination of mouthparts
and literature reviews.
All stable isotope samples were left to air dry and then dried for 48 hours in an oven at
60°C. Samples were then ground to powder using a ball mill (Retsch, Germany) and
weighed prior to stable isotope analysis.
Stable isotope analysis
Samples were analysed for δ13C and δ15N using a continuous flow system consisting of
a Delta V Plus stable isotope ratio mass spectrometer connected to a Thermo Flush
1112
via
Conflo
IV
(Thermo-Finnigan/Germany)
at
the Western
Australian
Biogeochemistry Centre at The University of Western Australia. The external errors of
analyses (1 std dev) were no more than 0.10 ‰ for δ13C and δ15N.
Multi-points normalisation was used to reduce raw values to fit the international scale
(Thompson et al. 2005; Paul et al. 2007). The values of international standards for
C (δ13C) were based on Coplen et al. (2006). All samples were standardised against
secondary reference samples (ANCA5 L-glut and WABC4 Glut), which were in turn
standardised against primary analytical standards obtained from the International
Atomic Energy Agency, Vienna (δ13C - NBS22, USGS24, NBS19, LSVEC; and for
δ15N - N1, N2, N3 and laboratory standards). All δ13C values are given in per mil
[‰, VPDB] and all δ15N values are given in per mil [‰, Air] according to delta notation
(Paul et al. 2007).
Data analysis
Community members were categorised into seven functional types: herbaceous
vegetation, non-herbaceous vegetation, leaf litter, invertebrate herbivores, invertebrate
carnivores, invertebrate omnivores and M. greyii. Stable isotope data for these
functional types were combined by habitat within locations for data analysis. Trophic
positions of each functional type were estimated graphically by plotting δ15N values
against δ13C values for habitat and habitat within location. The δ13C and δ15N values of
the functional types were compared between locations and habitats by permutational
analysis of variance (PERMANOVA).
Pair-wise post-hoc testing was used to assess for differences between the trophic
levels of the functional types within the three different habitats, with further testing of
interaction terms if necessary. Pair-wise post-hoc testing of the δ13C and δ15N values
41
for M. greyii used Monte Carlo simulations to assess probability levels due to the small
number of unique permutations of the data available for comparison. All analyses were
performed on untransformed data in a Euclidean distance-based similarity matrix. The
test incorporated two orthogonal fixed factors (location and habitat) with sites as
replicates tested with significance assessed by comparison against 9999 random
permutations of the data. These analysis were performed using the PRIMER-E
statistical package (version 6.1.13; Clarke & Gorely 2006) with the PERMANOVA+
add-on (version 1.0.3; Anderson et al. 2008).
RESULTS
All vegetation samples had δ13C values that were within the range of C3 plants (-20 ‰
to -35 ‰, Dawson et al. 2002; Bougoure et al. 2008). Woody species had a δ13C mean
range values of -30.4 ‰ to 28.4 ‰, across all sites and treatments. Similarly,
herbaceous species had a mean value of -29.5 ‰ to 30 ‰, and litter had a mean value
of -28.5 ‰ to 27.8 ‰ (Appendix I). When compared among the three habitats,
vegetation δ13C mean range values were slightly more dispersed in the sandalwood
plantation (-27.2 ‰ to -29.9 ‰), compared to the paddock (-28.8 ‰ to -29.2 ‰) and the
remnant vegetation (-27.4 ‰ to -28.3 ‰, Appendix II). However, vegetation δ13C mean
range values were more dispersed at Pingelly (-30.8 ‰ to -26.5 ‰) compared to Bokal
(-30.0 ‰ to -27.9 ‰) and Monjebup (-29.2 ‰ to -26.4 ‰) (Figure 10, Appendix III).This
observation is likely due to a greater abundance of more herbaceous species at
Pingelly, which in part reflects the early plantation age (1-2 years) at this site.
Owing to the narrow range of vegetation δ13C values, it was not possible to discriminate
primary food sources among sites or treatments (Figure 10). Consequently, subsequent
analyses focussed on using PERMANOVA tests on δ15N values to determine if trophic
structure differed among the three habitats (Table 10).
Across the three habitats, δ15N signatures of vegetation were generally highest
(i.e. most enriched) in the sandalwood plantation (although still close to 0 ‰) and
lowest (most depleted) in the remnant vegetation (Figure 10). There was a significant
effect of location x habitat on the δ15N values for the vegetation (Table 10).
42
LL
NHV
IO
HV
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
11
11
2
-1
HV
M.greyii
IO
IH
NHV
LL
-4
c)
δ15N [‰ AIR]
δ15N [‰ AIR]
14
5
2
-1
HV
δ13C [‰ VPDB]
δ13C [‰ VPDB]
14
11
11
M.greyii IO
5
IC
IH
HV
NHV
δ13C [‰ VPDB]
Bokal Sandalwood
11
5
2
NHV
-1
5
2
δ13C [‰ VPDB]
LL HV
IC
IO
M.greyii
-4
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
δ13C [‰ VPDB]
Monjebup Sandalwood
14
IO
8
-1
LL
15
IH
8
Monjebup Paddock
δ15N [‰ AIR]
δ15N [‰ AIR]
NHV
IO
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
2
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
-4
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
c
M.greyii
IH
5
14
-4
IC
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
8
NHV
14
8
Monjebup Remnant
-1
IO
HV
M.greyii
IO
Bokal Paddock
14
IC
M.greyii
IC IH
14
11
8
5
2
-1
-4
δ13C [‰ VPDB]
Bokal Remnant
8
IC
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
δ13C [‰ VPDB]
b)
Pingelly Sandalwood
IH
δ15N [‰ AIR]
M.greyii
14
11
8
5
2
-1
-4
δ15N [‰ AIR]
IH
Pingelly Paddock
δ15N [‰ AIR]
δ15N [‰ AIR]
Pingelly Remnant
14
11
8
5
2
-1
-4
HV
LL
IC M.greyii
IH
δ15N [‰ AIR]
a)
11
IC IO M.greyii
8
5
2
-1
IH
NHV
HV
-4
-4
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
-32 -31 -30 -29 -28 -27 -26 -25 -24 -23 -22
δ13C [‰ VPDB]
δ13C [‰ VPDB]
13
FIGURE 10: Plot of combined mean δ N against δ C (± SE) of trophic composition of secondary consumers in three habitats within study locations (a) Pingelly, (b) Bokal,
(c) Monjebup., NHV-Non herbaceous vegetation, HV-Herbaceous vegetation, LL-Leaf litter,. IH-Invertebrate herbivore, IC-Invertebrate carnivore, IO-Invertebrate omnivore.
42
43
TABLE 10: Permutational analysis of variance based on Euclidean distance, testing the
effect of location and habitat on δ15N values. P≤0.05*, P≤0.001**, P≤0.0001***, df =
degrees of freedom.
Number of
Functional
Source of
Mean
Pseudo-
types
variation
Vegetation
d.f.
Squares
F
P(perm)
permutations
Habitat
2
69.31
31.45
0.0001***
9965
Location
2
14.29
6.48
0.0031*
9952
Location x Habitat
4
15.3
6.94
0.0001***
9954
122
2.2
0.0396*
9951
Residuals
unique
Invertebrate
Habitat
2
24.83
3.7
Herbivores
Location
2
138.29
20.58
0.0001***
9950
Location x Habitat
4
3.19
0.48
0.7438
9957
Residuals
29
6.72
Invertebrate
Habitat
2
48.96
10.48
0.1958
9962
Carnivores
Location
2
8.31
1.78
0.1958
9962
Location x Habitat
3
5.55
1.19
0.3339
9956
Residuals
24
Invertebrate
Habitat
2
28.5
23
0.0001***
9954
Omnivores
Location
2
28.7
22.15
0.0001***
9954
Location x Habitat
4
2.31
1.79
0.1485
9932
Residuals
40
1.3
Habitat
2
16.67
14.16
0.0002**
9963
Location
2
13.96
11.86
0.0002**
9944
Location x Habitat
4
5.4
4.59
0.0039*
9951
Residuals
44
1.18
Menetia greyii
44
Pair-wise testing between locations within habitats indicated paddocks and sandalwood
plantations at Pingelly had higher δ15N values (1.9 ‰ to 2.9 ‰) compared to Bokal (0.5 ‰ to 0.7 ‰) and Monjebup (-1.6 ‰ to 1.7 ‰; Table 11a). Pair-wise testing between
habitats within locations indicated Pingelly had the highest δ15N values in sandalwood
plantations (1.7 ‰) and lowest in remnant habitat (-2.5 ‰ to 0.7 ‰), Bokal had higher
δ15N values in both paddocks (-0.5 ‰ to 0.6 ‰) and sandalwood plantations (-0.8 ‰ to
0.7 ‰) compared to remnant habitats (-1.9 ‰ to 0.4 ‰), Monjebup also had higher
δ15N values in both paddocks (-0.6‰ to 1.7 ‰) and sandalwood plantations (-1.6‰ to
0.2 ‰) compared to remnant habitat (-2.6 ‰ to 0.8 ‰; Table 11b). Overall the trend
appears that paddocks and sandalwood habitats had generally higher δ15N values and
the younger sandalwood plantations at Pingelly had higher δ15N values when compared
to the older sandlawood plantations at Bokal and Monjebup.
TABLE 11: Pair-wise post-hoc analysis within the interaction between location and
habitat for δ15N values of vegetation a) between locations within habitats and b)
between
habitats
Pad = Paddock,
within
San =
locations.
P = Pingelly,
Sandalwood,
Rem
=
B =
Bokal,
Remnant.
M = Monjebup.
P≤0.05*,
P≤0.001**,
P≤0.0001***.
a)
Habitat
Paddock
Sandalwood
Remnant
Location
t
P(perm)
P,B
4.74
0.0006**
P,M
2.89
B,M
b)
Location
Habitat
t
Pingelly
Pad, San
2.45
0.0371*
0.0112*
Pad, Rem
6.77
0.0001***
1.35
0.1841
San, Rem
5.59
0.0001***
P,B
4.36
0.0002**
Pad, San
0.31
0.7596
P,M
4.15
0.0015*
Pad, Rem
2.69
0.0116*
B,M
1.37
0.1851
San, Rem
3.36
0.0018**
P,B
1.19
0.2542
Pad, San
2.29
0.0334*
P,M
2.26
0.0297*
Pad, Rem
2.16
0.0380*
B,M
1.33
0.1911
San, Rem
0.02
0.9826
Bokal
Monjebup
P(perm)
Patterns in consumer δ15N values reflected those of vegetation and were most enriched
in the sandalwood plantation (7.3 ‰ to 9.1 ‰) and less enriched in the remnant
vegetation (4.9 ‰ to 6.3 ‰, Figure 10). Differences in δ15N enrichment between
consumer groups was highest in the invertebrate carnivores and M. greyii in the
sandalwood plantations (3 ‰ to 4 ‰) suggesting that sandalwood plantations has a
higher N source (Figure 10, Appendix II).
45
The δ15N values of herbivorous and omnivorous invertebrates differed with location and
habitat
(Table
10).
Pair-wise
testing
indicated
that
invertebrate
herbivores
(ants, Myrmecia spp.; small beetles, Scarabaeidae and Curculionidea; and small
crickets, Gryllidae) were generally more enriched in δ15N values in the sandalwood
plantations (8.5 ‰) compared to paddocks (7.6 ‰) and remnant vegetation (5.7 ‰). Of
the three locations, invertebrate herbivores at Pingelly had the highest δ15N values
(9.1 ‰ to 13.9 ‰, Table 12a). Invertebrate omnivores (ants, Camponotus spp.,
Iridomyrmex spp., Meranoplus spp. and Rhytidoponera spp.) showed the same general
trend as the invertebrate herbivores and were also more enriched in δ15N in
sandalwood plantations (7.3 ‰) compared to paddocks (6.3 ‰) and remnant vegetation
(4.9 ‰). Invertebrate omnivores at Monjebup had the highest δ15N values across the
three locations (6.1 ‰ to 8.6 ‰, Table 12b).
TABLE 12: Pair-wise post-hoc analysis of invertebrate δ15N values on Euclidean
distance-based similarity matrix between locations and between habitats (a)
Invertebrate Herbivore, (b) Invertebrate Omnivore. Pad = Paddock, San = Sandalwood,
Rem =
Remnant. P =
Pingelly, B = Bokal, M = Monjebup. P≤0.05*, P≤0.001**,
P≤0.0001***.
a)
t
Location
Habitat
P(perm)
b)
P(perm)
P,B
0.89
0.3755
P,B
4.26
0.0007**
P,M
6.02
0.0001***
P,M
4.76
0.0001***
B,M
1.47
0.1613
B,M
5.10
0.0001***
Pad, San
3.89
0.0006**
Pad, San
Location
t
Habitat
1.05
0.3056
Pad, Rem 1.60
0.1205
Pad, Rem
2.91
0.0068*
San, Rem 2.48
0.0225*
San, Rem
5.88
0.0002**
There was a significant interaction between location and habitat affecting the δ15N
values for the M. greyii (Table 10). Pair-wise testing indicated M. greyii in sandalwood
plantations had higher δ15N values (5.9 ‰ to 10.3 ‰) and similar δ15N values in the
paddock (6.2 ‰ to 7.1 ‰) and remnant vegetation (5.5 ‰ to 6.4 ‰, Table 13a). Pairwise testing between habitats within locations indicated M. greyii captured at Pingelly
and Monjebup had higher δ15N values in paddocks (7.1 ‰ and 6.2 ‰) and sandalwood
plantations (10.3 ‰ and 9 ‰), where M. greyii δ15N values at Bokal were similar
amongst the three habitats (5.5 ‰ to 6.2 ‰, Table 13b).
46
TABLE 13: Pair-wise post-hoc analysis within the interaction between location and
habitat for δ15N values of M. greyii a) between locations within habitats and b) between
habitats within locations. P =
Pingelly, B = Bokal, M = Monjebup. Pad = Paddock,
San = Sandalwood, Rem = Remnant. P≤0.05*, P≤0.001**. Probabilities are taken from
Monte Carlo simulations.
a)
Habitat
Paddock
Sandalwood
Remnant
Location
t
P(MC)
P,B
1.61
0.1199
P,M
1.25
B,M
b) Location
Habitat
t
P(MC)
Pad, San
3.72
0.0027*
0.2299
Pad, Rem
0.77
0.4487
0.19
0.8482
San, Rem
7.53
0.0024*
P,B
11.41
0.0005**
Pad, San
1.56
0.1561
P,M
2.37
0.0464*
Pad, Rem
0.98
0.3457
B,M
6.75
0.0002**
San, Rem
0.02
0.9892
P,B
0.83
0.4478
Pad, San
5.59
0.0005**
P,M
0.56
0.5756
Pad, Rem
0.50
0.6327
B,M
0.53
0.6138
San, Rem
5.35
0.0005**
Pingelly
Bokal
Monjebup
DISCUSSION
Menetia greyii is the top end consumer in this study and δ15N values were expected to
be significantly more enriched compared to primary producers and invertebrates.
Whilst this prediction held true for primary producers, it was not always the case with
the invertebrates. At Pingelly, M. greyii had higher δ15N values than the invertebrate
omnivores, but lower δ15N values when compared to invertebrate herbivores and
invertebrate carnivores across all three habitats. At Bokal, M.greyii’s δ15N values were
similar to invertebrates across the three habitats, suggesting food sources did not differ
significantly amongst the three habitats at Bokal. At Monjebup, M.greyii’s δ15N values
were generally slightly more enriched than those for the invertebrates, with the highest
δ15N values in the sandalwood plantation and similar δ15N values in the paddock and
remnant vegetation habitats.
Overall stable isotope results suggest that M.greyii exhibited an omnivorous diet in the
paddock and sandalwood plantation. In these two habitats there was little difference in
δ15N values between M. greyii and invertebrate omnivores (0.3 ‰ and 1.2 ‰,
respectively); this finding suggests that M. greyii feeds at a lower trophic level within
paddock and sandalwood plantation habitats. In the remnant vegetation, M. greyii
exhibited a more carnivorous diet with similar δ15N values to those of carnivorous
insects (6 ‰ and 6.3 ‰, respectively). This suggests that food webs are more complex
in the remnant vegetation compared to the paddock and sandalwood plantation, as
47
originally hypothesised. Whilst there was no change in M. greyii trophic position
amongst the three habitats, there seems to be a dietary shift amongst the three
habitats. This further implies that M.greyii diet makes it a highly adaptable skink that
can readily adjust to changes in landscapes.
M.greyii and invertebrates had the most depleted δ15N values (4.9 ‰ to 6.3 ‰) in the
remnant vegetation and higher δ15N values in the paddocks (6.3 ‰ to 7.5 ‰). This
could be attributable to paddock invertebrates not feeding solely on paddock
vegetation, but instead, feeding in the neighbouring sandalwood plantations where the
vegetation is more δ15N enriched. Alternatively, the invertebrates may also be
accessing other sources of nutrients not measured here, for example sap or nectar and
pollen of flowers (Blüthgen et al. 2003; Ottonetti et al. 2008; Hyodo et al. 2011
<online>). Invertebrate consumers could have then moved back into the paddocks
where they were eaten by M. greyii. Simultaneously, sandalwood invertebrates could
have dispersed into the paddocks where they were also eaten by M. greyii.
The most enriched δ15N values of M. greyii and invertebrates were detected in the
sandalwood plantations (7.3 ‰ to 9.1 ‰). Residual fertilizers retained in what was
previously agricultural land may have also contributed to the high δ15N values obtained
in sandalwood plantations. Excessive N availability can lead to increased N cycling
which increases δ15N in soil (Koerner et al. 1997; Koerner et al. 1999; Compton &
Boone 2000). Plants that are growing in this N pool can in time become δ15N enriched
(Dawson et al. 2002). The enriched δ15N would have accumulated in each trophic
transfer, further contributing to high δ15N values in M. greyii.
Studies investigating Acacia N-fixing properties have shown altered soil mineral
composition with elevated δ15N (e.g. Corbin & D' Antonio 2004; Lorenzo et al. 2010;
Hellmann et al. 2011; Isaac et al. 2011; Voigtlaender et al. 2012). Acacia species were
the majority of the mix native host plants in Bokal and Monjeup. At Pingelly
Acacia accuminata was the only host plant species. As acacias are legumes and
known N-fixers (Barker & Attiwill 1981; May & Attiwill 2003; McLauchlan 2006; Adams
et al. 2010), this may have also contributed to the higher δ15N values observed,
especially in Pingelly sandalwood plantations.
This study indicates sandalwood plantations have high δ15N values. This may be due to
an association with the soil micro-organism community that may have established as
the sandalwood plantation ages. Soil micro-organisms play an important role in
ecosystem functioning as they drive nutrient availability through N-fixation, retaining
48
soil fertility and decomposing detritus and plant residues (Power 2010). From this,
sandalwood plantations can have positive effects on other ecosystem services. Such
effects include increased diversity of plant community, providing resources for
pollinators and offering habitat and diverse food resources for invertebrates and
vertebrates (Tscharntke et al. 2005). With these flow on effects, it suggests rural
landscapes with sandalwood plantations could potentially offer an alternative habitat
resource that may benefit reptile ecology.
Whilst M. greyii appears to be a highly adaptable skink and is able to successfully
adjust to rural landscape changes through its diet, a comparison study would be
needed on more specialist reptiles to test whether these specialist reptiles exhibit
greater impacts on their trophic structure. Further investigation is also needed to better
understand trophic feeding shifts at the invertebrate consumer level and its effect on
higher level consumers. A study by Chikaraishi et al. (2011) highlights that δ15N values
of whole insects is only a starting point in beginning to understand insect trophic
relations and that compound specific analyses (i.e. amino acids) can help further clarify
trophic level food web interactions. By increasing the knowledge of what is transitioning
at each trophic level, it can assist in enabling better habitat management in a mixed
agricultural and agroforestry ecosystem.
49
CHAPTER 4
GENERAL DISCUSSION
Varanus gouldii in a southwest Australian wheat paddock.
This thesis evaluates the potential for profitable hardwood perennials (i.e. sandalwood
plantations) to enhance reptile biodiversity in the wheatbelt region of southwest
Australia. Findings from Chapter 2 indicated that young sandalwood plantations
(<10 years) lacked the habitat structural diversity needed to provide alternative
resources for reptiles. However, these young sandalwood plantations (<10 years) can
offer an extended resource for invertebrates, which make up the main diet of reptiles.
Chapter 3 took a closer look of trophic relations in an agricultural mixed agroforestry
landscape on a functional group level. Analysis showed a slight enrichment of trophic
level in sandalwood plantation, followed by paddock and then remnant vegetation. A
closer look at a generalist skink, Menetia greyii, showed no differences in trophic
position between the three habitats, but did appear to show a dietary shift.
Results from this study demonstrated sandalwood plantations can encourage the
recolonisation of generalist reptile species (Chapter 2). A review by Palacios et al.
(2013) found that in general, agroforestry systems of mostly mono-crops were
harbouring
herpetofauna
species
of
low
conservational
concern,
suggesting
homogenous plantations supported a substandard assemblage of generalist
herpetofauna species. While this study had similar findings, results also highlighted the
potential benefits sandalwood plantations with mixed host can have for the
conservation of specialist reptile species. Some specialist reptile species (Aprasia
repens, Lialis burtonis, Ramphotyphlops australis and R. waitii; Chapter 2) were found
to be utilising the sandalwood plantation with native mixed host plants. There was also
a suggestion that some terrestrial and fossorial reptile species were interchanging
between the remnant vegetation and sandalwood plantation with native mixed host
plants.
A possible explanation for specialist, terrestrial and fossorial reptile species utilising
sandalwood mixed host plantations could be the varied depths of leaf litter present,
which is an influential factor in the determination of reptile assemblage composition
(Craig et al. 2010). Reptile abundance is also often associated with understory and
ground layer (Brown 2001). Results from this study suggest that establishing
sandalwood plantations with native mixed host would further enhance floristic structure
and diversity, which may encourage the return of cryptic and specialised reptile species
into revegetated lands (Chapter 2). Craig et al. (2011) highlights the importance of the
presence of mature and specialised microhabitats as crucial in encouraging the return
of late-successional reptile species. However, these microhabitats take at least
100 years to develop, while sandalwood plantations can take 18-50 years to mature
(Rao et al. 2011; Smith et al. 2013). Although sandalwood plantations may never
51
support late-successional reptile species, they do have the potential to support
generalist and specialist reptile species (Chapter 2). Long-term monitoring of reptile
populations as sandalwood plantations age is needed to clarify if these plantations can
sustain existing reptile populations and encourage recolonisation of cryptic and
specialised reptile species.
Cunningham et al. (2007) and Hobbs et al. (2003a) concluded that plantations on
agricultural lands have the potential to improve habitat conditions for a few taxa. This is
most likely due to the lack of habitat complexity within these plantations. Low habitat
complexity has proven to be correlated with low faunal diversity, especially fauna
reliant on old-growth woodland habitats (Hobbs et al. 2003a; Cunningham et al. 2007).
This study shows that sandalwood mixed host plantations could provide habitat
complexity and potentially increase habitat diversity. As these plantations mature, they
will develop in structure, understory and vegetation diversity, thus providing future
extended habitat for existing reptile populations in agricultural lands.
Young sandalwood plantations (<10 years) are not as effective as remnant vegetation
in providing alternative habitat resources for reptiles. However, they do offer an
extended resource for invertebrate assemblages over paddocks. Sandalwood
plantations in this study had increased invertebrate abundance and higher richness
compared to paddocks (Chapter 2). This suggests invertebrate assemblages from this
study could increase in diversity when paddocks are planted with sandalwood mixed
host plantations. In a long-term revegetation study of 11 years, Haddad et al. (2011)
found encouraging plant diversity resulted in a more reliable food and habitat resource
for invertebrates. Thus, as the plantations in this study age, invertebrate assemblages
may revert towards those found in native remnant vegetation. Flow-on effects from
stable invertebrate populations may well be influential in increasing fauna diversity in
agricultural lands.
Several global studies indicate the retention of vegetation heterogeneity in agricultural
lands can play a considerable role in the persistence of many taxa of native fauna (e.g.
Glor et al. 2001; Mcadam et al. 2007; Sálek et al. 2009). This is due to fauna requiring
a variety of habitats during different life-stages, by utilising several habitats it allows
fauna to access different resources for growth and development (Law & Dickman
1998). Agroforestry ventures involving heterogeneous native plantations have been
shown to be beneficial in the establishment of native understory vegetation by
establishing a micro-climate that improves soil nutrients and enhance floristic
composition (Forrester et al. 2005; Nichols et al. 2006; Appiah 2012). Results from
52
Chapter 3 support the idea that mixed agroforestry plantations cultivate micro-climates
that improve soil nutrients.
The improvement of soil condition from sandalwood plantations with mixed host can
have positive effects on other ecosystem services. Sandalwood plantations in this
study had high δ15N values (7.3 ‰ to 9.1 ‰; Chapter 3). This may be due to a
combination of native mixed host plants and the cultivation of the soil micro-organism
community as the sandalwood plantation ages. However, further investigation is
needed to determine if this is the case. Improved soil fertility can increase plant
community diversity which in turn, encourages pollinators and offers a variety of habitat
and food resources for invertebrates and vertebrates (Tscharntke et al. 2005). This
suggests rural landscapes with mixed host plantations of sandalwood, could potentially
offer extended habitat resources that could benefit reptile and existing fauna
biodiversity.
Along with the need for habitat complexity, faunal mobility is also of great importance
for species persistence in agricultural landscapes (Smith et al. 2013). Bruton et al.
(2013) found that regrowth within 700 m of remnant vegetation was readily recolonised
by reptiles to the point where the reptile communities were similar to that in remnant
vegetation. In this study, sandalwood plantations were planted within 200-300 m of
remnant vegetation and this could explain the presence of some specialist reptile
species in sandalwood mixed host plantations (Chapter 2). Therefore, it is important to
consider design and placement of agroforestry plantations. Strategic placement of
agroforestry plantations can provide additional foraging and breeding sites for
generalist and specialist fauna and if appropriately placed, will not impact on existing
fauna that function on a smaller scale (McKenzie et al. 2013).
As most reptiles have low dispersal abilities (Fischer et al. 2003; Driscoll 2004; Fischer
et al. 2004), changes in habitat through land modification can have a major impact on
reptile health, habitat and food requirements (e.g. invertebrates). In this study, the
trophic position of a reptile was investigated using stable isotopes. While there are
many studies using stable isotopes in ecological research, approximately 72% of these
are aquatic based, less than 6% of studies focused on invertebrates and even fewer
studies (approximately 2%) concentrated on reptiles (Boecklen et al. 2011). Utilising
stable isotopes in terrestrial ecology can provide a non-invasive insight of trophic
structure interactions between trophic levels.
53
It is important to consider trophic relationships in biodiversity studies. Stable isotope
analysis can track how individuals shift feeding strategies under different management
regimes (Fry 2006). By focusing on an individual species, a general idea of how fauna
respond to short and long term management programs can be determined. In this
study, the cosmopolitan generalist skink, M. greyii, revealed no differences in its trophic
position between the three habitats (Chapter 3). However, M. greyii appeared to show a
dietary shift, switching from a carnivorous diet in more complex habitats (i.e. remnant
vegetation) to an omnivorous diet in less complex habitats (i.e. paddocks and
sandalwood plantation; Chapter 3).
The dietary switch reflects the finding that invertebrate assemblages had higher
abundance and richness in remnant vegetation (Chapter 2), thus offering a greater food
source variety compared to sandalwood plantations and paddocks. Menetia greyii in
this study has shown to be readily adaptable in modified lands (Chapter 3). This infers
generalist reptiles can rapidly adapt to altered landscapes over a short period of time.
However, the dietary shift in M. greyii also demonstrates the conservation value of
retaining remnant vegetation in agricultural landscapes. Using generalist species in
trophic level studies allows for a better understanding of ecosystem services. From this,
we can assess stability and resilience of ecological systems, which can then be used to
predict ecosystem responses to productivity and sustainability (Tixier et al. 2013).
Generalist species can be valuable study subjects in biodiversity and conservation
assessment. They can be utilised to investigate the viability of agroforestry plantations
in sustaining population health. Populations in poor heath can lead to population fitness
decline and a decrease in population size, accelerating local extinction (Schlaepfer et
al. 2002; Robertson et al. 2013). The study of generalist reptile species, which are
common and abundant, can assist in acquiring an overall evaluation of the biodiversity
status in landscapes. Investigating reptile health and body condition between habitats
could be a viable way for biodiversity status assessment. There are numerous noninvasive ways to assess reptile fitness and stress levels, including body condition
indices (e.g. Rotem et al. 2013) and carbon and nitrogen stable isotope analysis (e.g.
McCue & Pollock 2008).
It is no secret that biodiversity conservation on agricultural lands is a major ecological
concern worldwide. This has led to the re-evaluation of agroforestry and its potential
role in preserving and enhancing biodiversity in agricultural lands. Mixed agroforestry
plantations in agricultural landscapes can enhance fauna and flora biodiversity by
1) preventing further habitat degradation and loss, 2) creating and extending habitats,
54
3) conserving some rare and/or threatened plant species, 4) becoming important seed
banks for rare and/or threatened flora, and 5) controlling erosion and water recharge
(Woodall & Robinson 2003; Jose 2012). Results from this study have shown
sandalwood plantations with mixed host can support generalist reptile species and may
encourage recolonisation of specialist reptile species as plantations mature and
develop structural diversity and micro-habitats (Chapter 2, Chapter 3).
Reptiles were chosen as the focus taxa for this study as they
are known to be
ecologically restricted due to their sensitivity to habitat changes (Ribeiro et al. 2009).
The varied responses of reptiles to land disturbance and recovery makes them useful
in assessing habitat and biodiversity health (Bruton et al. 2013). As such, this trait has
led reptiles to be used as model organisms in ecological studies for over 30 years
(Luiselli 2008). However, despite their utility as model organisms, a global analysis by
Böhm et al. (2013) draws attention to the insufficient knowledge on reptile ecology. The
analysis revealed a reptile knowledge gap of 21% in data deficiency compared to birds
(1%) and mammals (15%).
From an agroforestry research perspective, only 15% of studies have focused on
herptofauna conservation and biodiversity (Palacios et al. 2013). The continual
monitoring of reptile populations in agroforestry schemes is an opportunity to close the
knowledge gap in reptile ecology. Reptiles have been shown to be model taxa for
ecological assessments and thus, they can be used to further assess the biodiversity
value of agroforestry schemes, especially during and after harvest. Only then, can we
aim to appropriately implement management strategies and policies. Effective land
management is an important first step in biodiversity conservation for all fauna that
inhabit agroforestry schemes and remaining natural vegetation on agricultural
landscapes.
55
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APPENDIX I: Stable isotope analysis of samples.
69
APPENDIX II: Stable isotope means (± SE) across the three habitats.
(a)
Remnant
Non herbaceous
vegetation
Herbaceous vegetation
Leaf litter
Invertebrate herbivore
Invertebrate carnivore
Invertebrate omnivore
Menetia greyii
(b)
Paddock
Non herbaceous
vegetation
7
1
8
1
5
n
Herbaceous vegetation
4
2
4
Leaf litter
3
Invertebrate herbivore
9
1
3
1
4
2
6
Invertebrate carnivore
Invertebrate omnivore
Menetia greyii
(c)
n
3
3
1
8
1
3
1
7
Sandalwood
Non herbaceous
vegetation
Herbaceous vegetation
Leaf litter
Invertebrate herbivore
Invertebrate carnivore
Invertebrate omnivore
Menetia greyii
n
2
0
1
0
6
1
1
1
2
1
7
1
2
δ13C
[‰VPDB]
-28.3 ±
0.3
-27.4 ±
0.3
-27.8 ±
0.3
-26.3 ±
0.5
-26.6 ±
0.7
-24.8 ±
0.2
-25.6 ±
0.2
δ13C
[‰VPDB]
-29.2 ±
0.2
-28.8 ±
0.2
-29.2 ±
0.2
-27.5 ±
1.1
-27.6 ±
0.6
δ15N
[‰AIR]
-1.9 ± 0.3
0.7 ± 0.2
-2.1 ± 0.4
5.7 ± 1
6.3 ± 1.1
4.9 ± 0.4
6 ± 0.3
δ15N
[‰AIR]
-0.5 ± 0.1
1.45 ± 0.3
-0.6 ± 0.3
7.6 ± 0.5
N [wt %]
11 ± 0.3
11.1 ±
0.4
C [wt %]
47.9 ±
0.9
45.6 ±
0.4
47.3 ±
0.8
49.8 ±
1.3
50.5 ±
2.3
48.6 ±
0.6
39.8 ±
1.6
N [wt %]
0.7 ±
0.05
C [wt %]
47.1 ±
1.8
1.5 ± 0.2
0.6 ±
0.01
44 ± 0.4
41.9 ±
0.1
44.3 ±
0.2
53.2 ±
1.6
46.7 ±
0.1
4.7 ± 0.4
41.3 ±1.3
3.7 ± 0.1
C [wt %]
47.6 ±
0.8
42.8 ±
0.6
46.8 ±
0.8
49.7 ±
1.5
C/N [wt]
1.4 ± 0.1
0.8 ±
0.06
1.1 ± 0.2
10.9 ±
0.4
13.1 ±
0.6
-26 ± 0.3
-26.3 ±
0.2
6.3 ± 0.4
6.6 ± 0.2
9.5 ± 0.2
10.4 ±
0.5
11.6 ±
0.3
11.4 ±
0.3
δ13C
[‰VPDB]
-29.9 ±
0.3
-27.2 ±
0.4
-28.5 ±
0.2
-26.8 ±
0.3
-26.7 ±
0.5
-25.3 ±
0.1
-25.4 ±
0.4
δ15N
[‰AIR]
N [wt %]
7.5 ± 0.7
0.5 ± 0.3
-0.01 ±
0.4
1.7 ± 0.1
0.1 ± 0.2
1.9 ± 0.1
11.3 ±
0.5
10.5 ±
0.8
11.4 ±
0.4
12.2 ±
0.5
8.5 ± 1.1
9.1 ± 0.9
7.3 ± 0.4
8.5 ± 0.6
0.5 ± 0.1
C/N [wt]
50.9 ± 5.4
65.1 ± 5
61.2 ±
10.7
4.7 ± 0.3
3.9 ± 0.3
4.4 ± 0.1
3.6 ± 0.1
C/N [wt]
64.1 ± 2.4
35 ± 3.2
68 ± 1.4
5.4 ± 0.5
4.1 ± 0.2
28.9 ± 1.3
106.7 ± 14
25.5 ± 1.3
4.4 ± 0.1
52.2 ± 2
49.6 ±
0.7
5.6 ± 0.8
42 ± 2
3.5 ± 0.3
4.4 ± 0.2
70
APPENDIX III: Stable isotope means (± SE) across the three study areas.
71
71