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New threats to endangered Cook’s scurvy grass
(Lepidium oleraceum; Brassicaceae): introduced crop
viruses and the extent of their spread
Josh C. C. M. Van Vianen
A,D
, Gary J. Houliston
B
, John D. Fletcher
C
, Peter B. Heenan
B
and Hazel M. Chapman
A
A
School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch 8140, New Zealand.
B
Manaaki Whenua-Landcare Research, PO Box 40, Lincoln 7640, New Zealand.
C
The New Zealand Institute for Plant & Food Research Ltd, Private Bag 4704, Christchurch, New Zealand.
D
Corresponding author. Email: josh.vanvianen@gmail.com
Abstract. To date, most research conducted on plant viruses has centred on agricultural systems where viruses greatly
reduce economic output. Introduced viruses are globally common and there is a lack of knowledge around how they might
affect natural populations. Although it has been suggested that infectious disease may have played an underestimated role
in past species extinctions, there is little empirical evidence. Cook’s scurvy grass (Lepidium oleraceum Sparrm. ex G.Forst;
Brassicaceae) is a threatened coastal plant endemic to New Zealand. Following the discovery of Turnip mosaic virus
(TuMV) in some glasshouse cultivated specimens, we surveyed wild extant Lepidium populations on the Otago coast for
TuMV while screening for two other common crop viruses. We show that TuMV is almost ubiquitous among remaining
wild L. oleraceum populations on the South Island’s east coast and report the first record of L. oleraceum as a host for both
Cauliflower mosaic virus and Turnip yellows virus. The high incidence of virus infection throughout the study populations
may make this system one of the first examples of introduced viruses affecting the conservation of a threatened plant species.
Additional keywords: biological invasions, CaMV, Lepidium oleraceum, New Zealand, plant conservation, TuMV, TuYV.
Received 17 October 2012, accepted 15 February 2013, published online 5 April 2013
Introduction
Cook’s scurvy grass, Lepidium oleraceum Sparrm. ex G.Forst;
Brassicaceae, named for its use by Captain James Cook as an
antiscorbutic for his crew during his voyages to New Zealand in
the 18th century (de Lange and Norton 1996), is one of six species
of coastal cress indigenous to New Zealand (Garnock-Jones
and Norton 1995; Norton and de Lange 1999). Five of these
are endemic, including L. oleraceum, and one is shared with
Tasmania (L. flexicaule; Hewson 1981). There has been a large
decline in both the range and distribution of coastal cress
populations, with all species being classified as extinct,
threatened with extinction or at risk under the revised New
Zealand Threat Classification System (de Lange et al. 2009).
The conservation status of these plants is of particular
significance to New Zealand plant conservation because of
historical records dating back to the first European explorers
who described the plants as being abundant and widely
distributed (Norton and de Lange 1999).
Lepidium oleraceum (threatened/nationally vulnerable) is
now estimated to be restricted to between 90 and 100 small,
isolated populations with many comprising less than 20
individuals. The total number of individuals is estimated to be
between 2000 and 5000 (Norton and de Lange 1999) and the
survival of the species is fully dependent on intensive
conservation management (de Lange et al. 2009).
Reasons for their decline include habitat degradation, the
loss of associated seabird and seal colonies, insect and fungal
pests, and browsing by introduced mammals (Norton and de
Lange 1999;
Hasenbank et
al. 2011). The discovery of Turnip
mosaic virus (TuMV; Family: Potyviridae Genus: Potyvirus)
in glasshouse specimens and in a replanted individual of
L. oleraceum from Banks Peninsula, Canterbury, New
Zealand, were the first records of any virus infecting this
species (Fletcher et al. 2009). This highlighted a potential new
threat to L. oleraceum.
TuMV is a common aphid-vectored virus of brassica and
other plant species in New Zealand, including: Armoracia
rusticana, Brassica napus, B. pekinensis, B. rapa, Erysimum
cheiri, Lunaria annua, Matthiola incana, Sinapis alba,
Sisymbrium officinale (Pearson et al. 2006), Rorippa
nasturtium-aquaticum (Anonymous 2004), Crocus sativus,
Erodium moschatum, Lobelia speciosa, Nasturtium officinale
and Tropaeolum majus (Ochoa Corona et al. 2007). TuMV
can cause symptoms of leaf mosaic, necrosis, chlorotic mottle
CSIRO PUBLISHING
Australian Journal of Botany, 2013, 61, 161–166
http://dx.doi.org/10.1071/BT12266
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and severe distortion as well as reductions in plant biomass
in important crop brassicas (Spence et al. 2007). In addition
TuMV has been known to reduce the fitness of wild brassicas
by reducing biomass, fecundity and survival (Maskell et al.
1999).
Most of the L. oleraceum individuals found to be infected
with TuMV in Fletcher et al.(2009) were either glasshouse-
grown research specimens or plants temporarily grown under
glasshouse conditions for replanting or conservation purposes. It
is possible that the plants were infected while under glasshouse
conditions where aphid infestations were common. These plants
were growing in close proximity to other TuMV host plants,
either in the glasshouses themselves (Fletcher et al. 2010)orin
the surrounding farming landscape. The Canterbury region is
dominated by agricultural land where brassica crops, grown in
abundance for human consumption and for sheep/cow fodder
provide a potential virus reservoir.
There is increasing interest in the role plant pathogens play
in regulating communities and ecosystem processes, with an
emphasis on the way in which anthropogenic climate change
may interact with plant-pathogen dynamics (Anderson and May
1986; Anderson et al. 2004; Garrett et al. 2006; Lafferty 2009).
In the case of viral pathogens, the bulk of the literature is
dominated by agricultural viruses and crop research where
viruses can have large impacts on economic outputs, with the
effects of plant viruses on natural systems rarely investigated
(Gilbert 2002). Nevertheless, there are examples of native
plants acting as hosts for introduced viruses (Pearson et al.
2006). Recent examples from New Zealand include the
infection of native grasses (Graminacae) with introduced
cereal and pasture grass viruses, namely, Cocksfoot mottle
virus, Barley yellow dwarf virus and Cereal yellow virus
(Davis and Guy 2001; Delmiglio et al. 2010 ) and Pachycladon
spp. with TuMV in glasshouse specimens (Fletcher et al. 2010).
Additionally, several broader-scale ecosystem level studies
have been carried out on the effect of viruses in natural
ecosystems in California (Malmstrom et al. 2005a, 2005b,
2006) and Australia (Webster et al. 2007). Despite some
research suggesting that pathogens may be an underestimated
factor contributing to global biodiversity loss (De Castro and
Bolker 2005; Smith
et al. 2006),
studies empirically stating
the effects introduced viruses may have on plant conservation
are scarce.
We surveyed the known remaining wild populations of
L. oleraceum on the South Island’s mainland east coast and
also tested one coastal population of L. tenuicaule Kirk, which
is currently classified as being at risk and declining (de Lange
et al. 2009). Because there is a plethora of introduced crop
viruses recorded in New Zealand (Pearson et al. 2006), we
have taken a targeted approach and surveyed two other
common brassica viruses; Cauliflower mosaic virus (CaMV;
Family: Caulimoviridae Genus: Caulimovirus), recorded in
New Zealand infecting six common crop brassicas including:
B. napus, B. napus var. napobrassica, B. oleracea var. botrytis,
B. oleracea var. capitata, B. oleracea var. ramosa, and B. rapa
(Pearson et al. 2006) and Turnip yellows virus (TuYV; Family:
Luteoviridae Genus: Polerovirus), with over 30 known hosts
in many plant genera including Brassicaceae (Pearson et al.
2006). Both of which we felt may also infect native Lepidium
hosts because of their wide host ranges, their common occurrence
in agricultural landscapes and a shared transmission pathway.
Materials and methods
Sample populations and species
Six populations of L. oleraceum were sampled, representing the
remaining known distribution of the species on the mainland
east coast of the South Island. These sites were Eye Tallus,
Highcliff, Long Beach and Aramoana in the vicinity of the
Otago Peninsula and Bridge Point and Tavora in North Otago.
Also sampled was one population of L. tenuicaule from Shag
Point, North Otago (Fig. 1). Although L. tenuicaule is currently
not a confirmed host for any viruses, being the same genus as
L. oleraceum it was included for testing as it may also be
susceptible to infection. Although there are other known
populations of Lepidium spp. distributed on offshore rock-
stacks such as Motunau Island off the Canterbury coast,
diffi
cult access prevented these populations being sampled.
Collection
of plant samples and storage
Sampling was conducted in March 2010. Because populations
were small, samples were collected from every individual adult
plant at each site except for L. tenuicaule at Shag Point where
a random subsample was taken so as to minimise impact on
the population. Virus symptoms often manifest visually as leaf
mosaic, necrosis, chlorotic mottle, leaf distortion and a reduced
plant biomass. Samples of between 3 and 5 leaves per plant
(5–10 g) were collected in equal proportions from both
symptomatic and asymptomatic stems and leaves. The
exception was L. tenuicaule, where because of their small size
and woody stems with small leaves, a larger number of leaves
were required. Leaves were stored in sealed plastic bags with a
small piece of moist tissue paper and kept cool with ice packs
then transferred to a 4
C fridge until processed.
Virus detection
Double antibody sandwich enzyme-linked immunosorbent
assay serological tests were conducted according to the
manufacturers’ protocols using two commercially available
kits and one prepared at Plant and Food Research: TuMV
(AS0132; DSMZ, Braunschweig, Germany), CaMV (AS0206;
DSMZ) and TuYV (Plant & Food Research g 048 coat and
conjugate). Duplicate samples of crushed leaf sap were tested,
with three negative and one positive control. Both positive and
negative control samples were obtained from B. napus (rape
seed), B. rapa var. rapa (turnip) or B. pekinensis (Bok Choi).
These were grown in glasshouse conditions at 18–22
C at Plant
& Food Research, Lincoln. Enzyme-linked immunosorbent
assay plates were coated with each antibody at appropriate
dilutions and incubated at 4
C overnight. Sample tissue was
crushed using a mechanised leaf roller then diluted with PBS-
Tween-PVP buffer (0.15 M phosphate-buffered saline, 0.05%
Tween 20, 2% polyvinylpyrrolidone 40) at a ratio of 1 : 10,
loaded on coated plates, then incubated. Conjugates were
diluted in PBS-Tween-PVP ovalbumen (0.2%): 1 mL/mL
(TuMV), 2 mL/mL (CaMV) and 2 mL/mL (TuYV). Plates were
washed 3 times for 3 min with PBS Tween buffer between
treatments. All incubations were carried out at 4
C overnight.
162 Australian Journal of Botany J. C. C. M. Van Vianen et al.
After incubation with the alkaline phosphatase conjugate, plates
were developed with 2,4 DNPP substrate (2,4 dinitrophenyl
phosphate; 0.5 mg/mL) and spectrometer readings were taken
at OD 405 nm at 30- and 60-min intervals. The threshold level
for a sample to be considered positive was when the A
405
reading from the spectrometer was greater than the mean value
of the negative controls plus 3 times the standard deviation.
Results
The results of the enzyme-linked immunosorbent assay tests on
Lepidium spp. are summarised in Table 1 and Fig. 1. Viruses were
detected in five of the seven populations. The L. oleraceum
population at Aramoana and the L. tenuicaule population at
Shag Point were virus-free. Of the 155 L. oleraceum plants
sampled, 75 (48.4%) were infected with viruses, of which 11
(14.6%) had multiple infections; one was co-infected with CaMV
and TuYV and the other 10 were co-infected with CaMV and
TuMV. Only two populations contained individuals displaying
obvious visual signs of viral infection with individuals at both
Long Beach and Tavora appearing to be symptomatic.
The most prevalent virus was CaMV, infecting 57 of the 155
(36.8%) L. oleraceum individuals sampled. TuMV was the next
most prevalent, infecting 28 of the 155 (18%) L. oleraceum
individuals sampled. In contrast, TuYV was only detected in
one individual L. oleraceum and it was a co-infection with
Tavora
Long Beach
8%
Highcliff
Bridge PointEye Tallus
Total Infected
TuMV +CaMV
TuMV
CaMV + TuYV
CaMV
Long Beach
Highcliff
Aramoana
Bridge Point
Shag Point
Tavora
Eye Tallus
Virus Free
Fig. 1. Map of New Zealand, showing the distribution of extant South Island east coast Otago Lepidium species and virus infection rates within
populations. All populations are L. oleraceum, except Shag Point (L. tenuicaule Kirk; excluded from total). Pie graphs show the virus community
composition within each Lepidium population and the total virus incidence across all populations for Turnip mosaic virus (TuMV), Cauliflower mosaic
virus (CaMV) and Turnip yellows virus (TuYV). Graphs for Shag Point and Aramoana are excluded because no viruses were detected.
Table 1. Virus population structure within Otago Lepidium populations
Data presented as counts of virus incidence including sum totals for each virus species and co-infections across all populations, the
proportion of infected individuals within each population and the presence of visual viral symptoms within each population. X, visual signs
of viral infection are present; TuMV, Turnip mosaic virus; CaMV, Cauliflower mosaic virus; TuYV, Turnip yellows virus
Population Population
size
Visual signs
of infection
present
TuMV CaMV TuYV TuMV
+
CaMV
CaMV
+
TuYV
Total
infected
Eye Tallus
A
16 – 110 – 1 – 75%
Tavora
A
77 X 10 35 – 7 – 68%
Bridge Point
A
6 – 1 –– 2 – 50%
Long Beach
A
31 X 6 1 –––23%
Highcliff
A
12 –––––18%
Aramoana
A
13 –––––––
Shag Point
B
9 –––––––
Total
C
155 – 18 46 – 10 1 48%
A
Lepidium oleraceum.
B
Lepidium tenuicaule Kirk (~10% of true population size).
C
Does not include Shag Point population.
New threats to endangered Cook’s scurvy grass Australian Journal of Botany 163
CaMV. The A
405
reading for the TuYV was only just higher
than the threshold and so was determined as being only weakly
positive for TuYV.
Aramoana was the only L. oleraceum population where
virus was not detected. Across the other populations infection
rates ranged from 8% at Highcliff to 75% at Eye Tallus. All
infected L. oleraceum populations had at least two virus species
present.
Discussion
Virus distribution
This study has shown that three introduced viruses infecting
brassica crops are prevalent among New Zealand’s endemic
L. oleraceum populations on the Otago coast. Infection rates
ranged from 8 to 75% in all populations apart from Aramoana
where virus was not detected. These levels of infection are
similar to those of TuMV, CaMV and TuYV in natural
B. oleracea populations in southern England, where their
incidence is reported to range between 16 and 90% (Raybould
et al. 1999). The three virus species detected in this study had
varying levels of incidence across all the L. oleraceum
populations. Both the proportion of infected plants and the
structure of the virus community varied within each
population. For example, the virus community structure in the
Tavora population was dominated by CaMV infection (68%),
followed by TuMV (19%) and co-infection with both (13%).
In contrast, the structure of the virus community in the Long
Beach population was dominated by TuMV (86%), followed
by CaMV (14%) with no co-infections occurring (Table 1,
Fig. 1). Possible reasons for variation in virus incidence
between population sites and among individual plants may
include: genetic variation in host plant pathogen resistance
(Hammond-Kosack and Jones 1996; Parker and Gilbert 2004);
variation in vector density, herbivory and behaviour (Carmona
et al. 2011); the proximity of virus source populations, cultivated
or wild (De Castro and Bolker 2005; Malmstrom et al. 2005b);
the demographic structure of the host population (Raybould
et al. 1999); interactions between viruses (Power 1996); and a
wide range of climatic and environmental variables (Coakley
et al. 1999; Chakraborty et al. 2000; Garrett et al. 2006).
Among the surveyed populations, not all expressed virus
symptoms. For example, it was noted that the Long Beach and
Tavora populations were observed to have obvious and often
systemic virus symptoms. In contrast, the Bridge Point, Eye
Tallus and Highcliff populations were not noted as having
obvious visual symptoms, yet also tested positive for virus
infection. This could suggest that there may be some natural/
evolved tolerance or resistance to infection among some
Lepidium populations. The Aramoana population is
geographically similar and in close proximity (~6 km) to Long
Beach, where 23% of the population is infected, therefore one
would also expect to detect viruses at Aramoana. The complete
lack of virus infection at Aramoana might be explained by
harsher environmental conditions and the resulting changes in
plant morphology. This population inhabits a man-made break-
water where high winds and sea spray are constant features. This
is reflected in the plant adaptations of thick waxy leaves and a
woody, prostrate habit. These characteristics, combined with
potentially suboptimal environmental conditions for aphid
vectors and other potential host plants, may be contributing
factors explaining why this population has remained virus-free.
While the Shag Point L. tenuicaule population shares the
same geographic and landscape characteristics as the other
populations, it also appears virus-free and elsewhere has not
been recorded as a virus host. There may be some biological
reasons for viruses not occurring in L. tenuicaule that relate to
its phylogenetic history. Lepidium in
New Zealand comprises
two lineages (Mitchell and Heenan 2000; Mummenhoff et al.
2004) with L. oleraceum in one lineage and L. tenuicaule in
another. Another reason could be a sampling effect. Unlike
the L. oleraceum populations, where every individual in each
population was sampled, at Shag Point only a random subsample
of nine plants representing ~10% of the population was taken so
as to minimise negative impacts on the population. Although
all sampled individual plants lacked any observable virus
symptoms and tested negative for virus in the laboratory, this
does not conclusively exclude the possibility that the three virus
species we tested for, or any other viruses, are present in the
population. A further observation was that large aphid colonies
were present in most L. oleraceum populations during sample
collection; however, no aphids were observed feeding on
L. tenuicaule. These observations may re flect differences in
the host preference of aphid vectors, related to morphological
differences between the species. In comparison to the erect
(>50 cm), bright green fleshy-leafed L. oleraceum,
L. tenuicaule is a much smaller, prostrate species with small
pinnate leaves (Norton and de Lange 1999). This may be a
contributing factor to this population remaining virus-free.
Further study is needed to determine if L. tenuicaule is indeed
a target species for known aphid vectors and thus potentially a
viable host for these viruses.
Virus establishment at the Tavora population may have a
different history to the other sites. This population has been
replanted as part of a wider coastal ecosystem restoration
project, with plants derived from seed collected on other parts
of the Otago coast. While the virus species detected in this
study are not known to be seed transmitted, it is possible that
infection occurred during propagation of seedlings in the
glasshouse or shade house. This may have influenced the
infection rate in this population, as the majority of individuals
in the Tavora population are of the same or similar age and age
class structure has been shown to be a determinant of virus
infection rates (Raybould et al. 1999; Spence et al. 2007).
Multiple infections
Our data shows that multiple infections – that is, individuals
infected with more than one virus species – are common. In total,
14.6% of all infected individuals in this study were co-infected.
This is a typical phenomenon, which has been reported in several
other plant virus studies (Raybould et al. 1999; Davis and Guy
2001; Syller 2012). Multiple virus infections can lead to a variety
of intra-host virus-virus interactions, both antagonistic and
synergistic (García-Cano et al. 2006; Mukasa et al. 2006;
Spence et al. 2007; Syller 2012).
Different viruses can also exert differential forces on disease
transmission by altering vector preferences for hosts infected with
164 Australian Journal of Botany J. C. C. M. Van Vianen et al.
certain viruses over others. For example, aphids settling
preferentially on virus-infected host plants or producing more
offspring on infected hosts (Bosque-Pérez and Eigenbrode
2011). Understanding which factors are responsible for
determining the virus community structure and how the
viruses are affecting the persistence of L. oleraceum
populations is a matter for further research.
Future research and implications for management
The implications of this study are wide ranging in terms of
both the conservation of New Zealand’s coastal cresses and
the future direction of plant conservation in general. Although
these populations have high levels of viral infection, we do not
know how these viruses are affecting plant fitness, ecology or
population survival. Lepidium oleraceum is a relatively short-
lived (5–10 years) perennial herb, which flowers readily and
produces an abundance of small seed on which it is reliant
for propagation (Norton and de Lange 1999). Historically
L. oleraceum has been associated with the high soil fertility of
sea bird colonies (Norton et al. 1997). The loss of such habitat,
coupled with high natural variation in population size (Norton
and de Lange 1999; de Lange et al. 2009) makes this species
especially vulnerable to loss of fitness through reduced seed
production or increased mortality rates from viral infection.
Such negative influences will have large implications for its
conservation. While this is a preliminary study and we are yet
to measure the direct effect of viral infection in L. oleraceum,
we can surmise that because effects such as reduced biomass,
reduced seed output and increased mortality are common
responses in other brassicas infected with the same virus
species (Maskell et al. 1999; Spence et al. 2007), there is a
high likelihood L. oleraceum populations on the Otago coastline
are suffering from similarly negative effects associated with
virus infection. With this in mind, steps have been taken to
ensure conservation nursery staff are now aware of the risks of
introducing virus-infected plants (Fletcher et al. 2009). Though
there are other examples of introduced plants acting as reservoirs
for common viruses leading to the infection of natives, such as
the discovery of the Barley yellow dwarf virus, Cereal yellow
dwarf virus and Cocksfoot mottle virus infections in several native
New Zealand grasses (Delmiglio et al. 2010), virus infections in
Lepidium may be the first example of introduced viruses directly
affecting the conservation of an endangered species.
Understanding the role of infectious diseases in species
extinction is a growing field of research. Global change has
already been shown to increase the transmission of infectious
diseases worldwide (Garrett et al. 2006
), with potential
consequences
for native plant populations (Jones 2009). Smith
et al.(2006) state that ‘it is critical that we combine evidence
with theory to discern the circumstances under which infectious
disease is most likely to serve as an agent of extinction’.
Unfortunately, in the case of L. oleraceum, theory predicts that
a combination of small population sizes, potential inbreeding
depression, the presence of virus reservoirs and the vector-
transmitted nature of the viruses are all potential contributing
factors leading to disease-induced extinction (De Castro and
Bolker 2005). Following the Smith et al.(2006) call for
combining theory and evidence, and given the conservation
status of these endemic New Zealand plants, it is imperative
that future research concentrates on quantifying the effects that
these viruses are having on both individual plant fitness and
population persistence. This survey is important in that it
demonstrates for the first time that infection from introduced
viruses is a threat to the survival of New Zealand’s coastal
cresses. Future studies should incorporate viral molecular
systematics to elucidate evolutionary processes which may be
affecting the pathogenicity of these viruses of Lepidium.In
addition, as all three common crop viruses we tested for infect
native hosts, it is important to carry out wider surveys to
understand the scale of viral threats to native New Zealand
plant species. The cosmopolitan nature of crop viruses of the
type discussed in this study may also warrant further
investigation into declines of native Lepidium species in other
countries. For example, there are six species of Lepidium in
Australia listed as being endangered, vulnerable or poorly
known (Briggs and Leigh 1996). These species may also be
suffering from and/or be at risk of viral infection, especially if
they are restricted to landscapes with historical and widespread
agricultural land conversion such as those dominating the South
Island of New Zealand.
Acknowledgements
This work was supported by the MBIE-funded research program C09X0503
to Landcare Research and The Better Border Biosecurity(B3) program funded
by MSI (JF). We would also like to thank Graeme Loh, John Barkla and the
Department of Conservation for sampling permission and the guided tour of
Otago Peninsula.
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