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2006 SOUTHEASTERN NATURALIST 5(1):103–112
Rudbeckia auriculata Infected with a Pollen-mimic Fungus
ALVIN R. DIAMOND, JR.1,*, HANAN EL MAYAS2, AND ROBERT S. BOYD3
Abstract - The fungus Fusarium semitectum infects the flowering heads of Rudbeckia
auriculata at two sites in Alabama. This is the first report of a fungal agent
infecting this globally rare species. The fungus produces orange-tinged or pinkishwhite
spores on the flower heads and renders infected flowers sterile. Fungal spores
superficially resembled pollen and are picked up by the main pollinator, the composite
specialist bee Andrena aliciae, which serves as a dispersal agent for the fungal
pathogen. Fungal spores were found attached in higher ratios in those areas of the
bee’s body that come into most direct contact with the flowering heads during
feeding. The rate of spread of the fungus on potted plants indicated significant
negative correlations between number of infections and the distance from the fungal
source. Fusarium colonies were isolated from the entire length of flowering stems,
and apparently invade vegetative portions of the plants. As R. auriculata is a
perennial plant that reproduces almost exclusively by the production of short stolons,
the fungus poses no serious threat to its immediate existence.
Fungi that alter floral parts or vegetative portions of plants to resemble
flowers (pseudo-flowers) in order to dupe insects into acting as vectors for
their spores have been reported in many species of plants. Insect pollinators
have been identified as agents of dispersal for fungal pathogens in Silene
(Atonovics and Alexander 1992, Baker 1947, Real et al. 1992, Soldatt and
Vetter 1995, Thrall et al. 1993), several species of Cruciferae (Roy 1993,
1996), Euphorbia cyparissias L. (Pfunder and Roy 2000), and members of
the Ericaceae (Batra 1991, Batra and Batra 1985). This relationship may be
quite common (Roy 1996).
Perhaps the most familiar case of floral mimicry is that of the rust
Puccinia monoica (Peck) Arth., which infects species of crucifers and
grasses (Roy 1993, 1996). The fungus prevents the infected host plant from
flowering and causes it to produce pseudo-flowers from vegetative tissues
that resemble flowers of other species in size, color, shape, scent, and nectar
production (Roy 1993). Species of Ustilago infect at least 92 species of
caryophyllaceous plants in Europe and 21 in North America (Delmotte et al.
1999, Skogsmyr 1993, Skykoff and Bucheli 1995, Soldaat and Vetter 1995,
Thrall et al. 1993), rendering the plants sterile the next season when fungal
spores are produced instead of pollen (Skogsmyr 1993). In the genus
1Department of Biological and Environmental Sciences, 210K McCall Hall, Troy
University, Troy, AL 36082. 2Department of Biology, Georgia State University,
Atlanta, GA 30303. 3Department of Biological Sciences, 101 Life Sciences Building,
Auburn University, Auburn, AL 36849. *Corresponding author - firstname.lastname@example.org.
104 Southeastern Naturalist Vol. 5, No. 1
Vaccinium, the fungus Monilinia infects flowers, fruit, and shoots. Infected
tissues are ultraviolet reflective, fragrant, and produce sugar secretions that
attract insects (Caruso and Ramsdell 1995). In all instances, insect visitors to
otherwise healthy plants spread the fungal pathogen.
During fieldwork on investigations of insect pollinators of Rudbeckia
auriculata (Perdue) Kral in 1999, a fungus was observed infecting flower
heads at a site in Crenshaw County, AL (31°43'42"N, 86°19'33"W). In 2001,
the same fungus was observed infecting flower heads at a second population
located approximately 84 km to the south in Covington County, AL
(31°02'23"N, 86°13'07"W). The fungus was identified by plant pathologists
at Auburn University as Fusarium semitectum Berk. & Ravenel, a common
soil fungus that infects many plant species worldwide (Dhingra and
Muchovej 1979, Marin-Sanchez and Jimenez-Diaz 1982, Nedumaran and
Vidyasekaran 1982, Singh et al. 1983). Fusarium species cause cereal ear
blight in grain crops and have been reported to infect other species such as
Nicotiana tabacum L. (tobacco), Solanum lycopersicum L. (tomato), Glycine
max (L.) Merr. (soybean), and Arabidopsis, where disease symptoms
were produced in anthers, filaments, and petals (Urban et al. 2002).
Fusarium semitectum produced orangish or pinkish-white spores that
superficially resembled pollen on the R. auriculata flower heads (Fig. 1).
Figure 1. Rudbeckia auriculata showing head with normal flowers (yellow pollen)
and flowers infected with Fusarium semitectum (pinkish-white).
2006 A.R. Diamond, Jr., H. El Mayas, and R.S. Boyd 105
The appearance of infected flowers was similar to the appearance of
Fusarium head blight on small grain crops (McMullen and Stack 1999).
Individual flowers on which fungal spores developed did not produce pollen
or seeds and were, in effect, sterile. The disc flowers of R. auriculata are
dark purplish-black, and both the pollen grains and fungal spores are clearly
visible. Upon closer inspection it is not difficult to distinguish the fungal
spores from the golden yellow pollen. However, in the field, insects were
observed to land on the infected heads and walk over them for short periods
of time before flying to another head on the same or a different plant.
Examination of pollen removed from insect visitors revealed fungal spores
along with Rudbeckia pollen.
Rudbeckia auriculata flower heads infected with the fungus were collected
in 1999 to determine if the fungus could be transferred to healthy
plants. The infected heads were lightly touched to heads of 5 individual
plants grown in Pike County, AL, from seed collected from populations in
which the fungus had not been observed. Within 2–4 weeks, the fungus was
observed on most of the heads that had been exposed to the fungus.
Next we sought to determine: (1) if the fungus was present in the
vegetative portions of stems below infected flowering heads, (2) the average
fungal spore load and location of the spores on the body of the most
important floral visitor, (3) the ratios of fungal spores to pollen grains on
various areas of the body of the most important floral visitor, and (4) the rate
of spread of this pathogen.
Rudbeckia auriculata is listed as critically imperiled globally and critically
imperiled within their states by the Alabama and Georgia Natural Heritage
Programs (ANHP 2004, GNHP 2004). It is known from only one county in
Georgia and 10 counties in Alabama, where populations are small and vulnerable
to human disturbance (Diamond and Boyd 2004). Any agent responsible
for decreased reproductive success could negatively impact this rare species.
Materials and Methods
In order to determine if the fungus was present in vegetative portions of
infected plants, entire stems with infected flowering heads were removed
at ground level from the Crenshaw County site. The leaves and flowering
heads were removed and the stems were then washed with running water
and surface sterilized by dipping for 2–3 minutes in 1% sodium hypochlorite
in 10% ethanol. After rinsing with sterile water, the stems were cut into
5 mm longitudinal sections with sterile blades. These stem sections were
placed in 100 ml sterile water and shaken vigorously for 1 minute. Afterwards,
0.5 ml of the dilution was spread on the selective medium,
dichloran chloramphenicol peptone agar (DCPA; Burgess et al. 1988), that
contains the growth retardant dichloran (Botran®), which delays the growth
of other fungal genera but allows sporulation of Fusarium species, and
chloramphenicol, an autoclavable antibiotic that prevents bacterial growth.
Fungal identifications were made utilizing the Synoptic FusKey Fusarium
106 Southeastern Naturalist Vol. 5, No. 1
interactive key (Agriculture and Agri-Food Canada 2000), and keys by
Burgess et al. (1988) and Nelson et al. (1983).
The most common insect species collected from R. auriculata was
Andrena aliciae Robertson, which was also the principal pollinator, transporting
a majority of the pollen (Diamond and Boyd 2004). Most other
species collected at the study site carried little or no pollen and were far less
common (Diamond and Boyd 2004). For that reason, we chose to focus this
study on A. aliciae.
The Andrenid bees were collected with a standard insect net while they
were on un-infected flowering heads of R. auriculata at the study site in
Crenshaw County during peak flowering in 2002. Insects were captured,
placed in a kill jar, and then transferred by forceps to individual vials. Vials
were stored in a standard freezer. Pollen/fungal spore samples were removed
from 20 bees chosen arbitrarily. Six areas on each bee were sampled utilizing
individual 2-mm2 glycerin gel squares: face, top of thorax, bottom of
thorax, top of abdomen, bottom of abdomen, and legs/feet. The gel was
affixed to a slide and the total number of pollen grains and fungal spores
were counted for each sample area for each insect.
Correlation analysis was performed to determine if there were significant
differences in the ratio of pollen grains to fungal spores on sampled areas of
the insects’ bodies. Data were also analyzed to determine if significant
variances existed in the number of pollen grains and fungal spores on
different areas of the insects’ bodies: i.e., are some areas better at carrying
pollen and others better at fungal transmission. Both the raw data and the
ratio of fungal spores to pollen grains were analyzed. Due to a violation of
the assumption of sphericity, as indicated by Levine’s test, a non-parametric
Kruskal-Wallis test was performed.
Ninety pots of R. auriculata plants were grown from achenes collected in
populations in which the fungus had not been observed to determine the
rates of spread of this fungus. Achenes were scattered on the soil surface in
3.8-L black plastic nursery pots filled to within 2.5 cm of the lip with Sam’s
Choice® potting soil. The pots were placed in aluminum pans filled with
rainwater that were 12.7 cm deep. The plants were 4 years old from seed, and
each had flowered at least twice with no evidence of the fungus being
present. Plants for the experiment were chosen arbitrarily.
Three experiments were undertaken during the summer of 2003. In the
first experiment, flower heads infected in Crenshaw County were brought
back to Pike County to determine the distance the fungus could spread to uninfected
plants by insect visitors or other vectors (e.g., wind, rain) in an area
free of the fungus. In the first experiment, the infected flower heads were
placed in a bottle of water at the same height as the inflorescence of 12 R.
auriculata plants. The infected heads were in the center of the potted plants
located edge to edge, with 3 pots aligned in each of the cardinal compass
directions. The outside edge of the outer pots was 53 cm from the fungal
source. Three replicates of this setup were arrayed for a total of 36 plants.
2006 A.R. Diamond, Jr., H. El Mayas, and R.S. Boyd 107
The heads infected with the fungus were replaced with freshly collected
heads when they began to show signs of age.
In the second experiment, flower heads infected with the fungus were
again placed in a bottle of water in the center of 12 R. auriculata plants, again
arrayed in cardinal compass directions. This time the inside edge of the pots
were 61 cm, 122 cm, and 244 cm from the fungus in each direction. Three
replicates of this experiment were run for a total of 36 R. auriculata plants.
In the third experiment, uninfected potted plants were placed in the
infected population in Crenshaw County to determine the distance that the
fungus could spread to un-infected plants in an area with a high concentration
of fungal spores available. Three pots were placed in the center of infected
clumps, three along the edge of the infected population, and three pots 6 m
from the nearest infected plant. Two replicates were run for a total of 18 pots.
At the end of the flowering period, as determined by the withering of the
ray flowers, the numbers of heads with the fungus visible were counted at
each distance from the fungal source. The heads were harvested and the
number of individual flowers infected was counted for each distance from
the source. Data were analyzed utilizing the non-parametric Spearman’s
correlation. All statistical analysis was performed using SPSS 11.5 for
Windows with an α = 0.05.
Fusarium semitectum colonies were isolated from the entire length of the
stems. Isolated colonies were identical to colonies isolated from infected
flowers. Conidial masses on potato dextrose agar (PDA) were pale orange
with aerial mycelium abundant. The reverse colony color on PDA was cream
to salmon orange. Colonies grew rapidly (3 cm after 3 days) and produced a
fruity odor. Two types of macroconidia were observed. Macroconidia from
sporodochia obtained after 10–11 days of growth on the low nutrient medium
synthetischer nährstoffärmer agar (SNA) were sickle-shaped, straight to
slightly curved with 4–5 (rarely 6) septa equally distant. The apical cell was
conical, curved at the end, and penultimate. The basal cell was slightly
notched. Macroconidia varied considerably, but averaged 75 μm in length and
3.7 μm in width (n = 13). Macroconidia formed from the aerial mycelium on
polyphialides were straight and spindle shaped, with 2–3 septa. Microconidia
formed either singularly on a monophialide or in false heads at the tips of the
conidiogenous cells (= conidiophore). Microconidia were aseptate or had 1
septum, and averaged 14.2 μm in length. They were abundantly produced in
false heads, mainly from polyphialides, but also from monophialides.
Fungal spores were isolated from all 20 bees. Spores were found attached to
the bodies of the andrenid bees in higher ratios in those areas of the bee’s body
that come into most direct contact with the flowering heads during feeding
(Table 1). The Kruskal-Wallis test demonstrated a significant variance in the
ratio of pollen to fungal spores for different areas of the bees’ bodies, both for
the raw data and the fungal spore/pollen grain ratios. The pollen and fungal
108 Southeastern Naturalist Vol. 5, No. 1
Table 1. Numbers of Rudbeckia auriculata pollen grains and Fusarium semitectum fungal
spores from various locations on the bodies of Andrena aliciae bees collected on R. auriculata
plants in Crenshaw County, AL. The Kruskal-Wallis test demonstrated a significant variance in
the ratio of pollen to fungal spores for different areas of the bees’ bodies: Raw data: χ2 = 88.1,
df = 5, p < 0.001 for pollen grains and χ2 = 21.6, df = 5, p = 0.001 for fungal spores; Ratio data:
χ2 = 5.1, df = 5, p = 0.408.
Location Pollen grains Fungal spores Ratio
Lower thorax 34,218 522 66:1
Upper thorax 9,660 105 92:1
Lower abdomen 57,678 1090 53:1
Upper abdomen 27,373 445 66:1
Face 15,474 347 45:1
Legs 90,344 2490 36:1
Total 234,747 4999 47:1
Table 2. Mean number and SD for Rudbeckia auriculata heads and flowers infected with
Fusarium semitectum in pots located edge to edge. The rate of spread of the fungus indicated
significant negative correlations between number of infections and the distance from the fungal
source (Spearman’s correlation: heads: -0.475, p = 0.003; flowers: -0.499, p = 0.002).
Distance from infection Mean number of Mean number of
source to center of pot infected heads infected flowers
9 cm 1.83, SD = 1.01 7.74, SD = 2.58
27 cm 0.83, SD = 0.52 4.53, SD = 1.50
45 cm 0.17, SD = 0.29 1.00, SD = 1.73
Table 3. Mean number and SD for Rudbeckia auriculata heads and flowers infected with
Fusarium semitectum in pots with the inside edge of the pots 61 cm, 122 cm, and 244 cm from
the fungus direction. The rate of spread of the fungus indicated significant negative correlations
between number of infections and the distance from the fungal source (Spearman’s correlation:
heads: -0.390, p = 0.019; flowers: -0.387, p = 0.020).
Distance from Mean number of Mean number of
infection source infected heads infected flowers
61 cm 0.67, SD = 0.38 2.95, SD = 0.32
122 cm 0.17, SD = 0.29 1.00, SD = 1.73
244 cm 0.00 0.00
Table 4. Mean and SD for Rudbeckia auriculata heads and flowers infected with Fusarium
semitectum on potted plants placed in the middle, at the edge, and 6 m from the nearest infected
clump of Rudbeckia auriculata plants in Crenshaw County, AL. The rate of spread of the fungus
indicated significant negative correlations between number of infections and the distance from
the fungal source (Spearman’s correlation: heads: -0.861, p < 0.001; flowers: -0.873, p < 0.001).
Location relative to Mean number of Mean number of
infected population infected heads infected flowers
Middle 5.00, SD = 0.42 9.68, SD = 0.81
Edge 1.25, SD = 0.35 6.14, SD = 0.91
6 m 0.00 0.00
spore load varied in the same order, with pollen load being greater on all sites
than fungal spore load (Table 1). Analysis of the data on the rate of spread of the
2006 A.R. Diamond, Jr., H. El Mayas, and R.S. Boyd 109
fungus on potted plants indicated significant negative correlations between
number of infections and the distance from the fungal source (Tables 2, 3, 4).
In an experiment in which Rudbeckia heads were bagged with an insectproof
material, significantly fewer seeds were produced than in open
pollinated heads (Diamond and Boyd 2004), indicating that insects are critical
for pollination of this species. However, insects are transmitting not only
pollen but also fungal spores that could infect the flowers and render them
sterile. The plant-pollinator mutualism appears to be exploited by the fungus,
which mimics pollen to attract insects that then disseminate its spores.
The fitness of R. auriculata is reduced by infection with the plant pathogen
F. semitectum, since infected flowers fail to produce seeds. In the
natural populations, approximately 3–5% of the plants contained at least
some flower heads infected with the fungus. Infection rates within heads
varied from a single flower to as much as the entire head, but were generally
in the 5–10% infected range. This is less than the 20–48% infection rate for
plants of Euphorbia cyparissias, although infection rates have been reported
to vary between populations and between years (Lara and Ornelas 2003,
Pfunder and Roy 2000). Other investigators have reported extremely low
infection rates for plants of Silene virginica L. (Antonovics et al. 1996) and
low transmission rates within long-established populations of Silene alba (P.
Mill.) Krause (Alexander and Antonovics 1995). Low infection and transmission
rates in R. auriculata may be due to resistant genotypes as has been
demonstrated in Silene alba (Mill.) J. Krause (Alexander and Antonovics
1995). As R. auriculata is a perennial plant that reproduces almost exclusively
by the production of short stolons (Diamond and Boyd 2004), the
fungus poses no serious immediate threat to local populations, and most
populations remain free of infection by the fungus at this time.
Evidence indicates that the fungus can invade the perennial parts of the R.
auriculata plants via the stem, and that initial infection results in at least some
of the plants producing diseased flower heads in subsequent years. Fusarium
colonies were isolated from the entire length of stems that were producing
infected flower heads. Three of five plants infected with the fungus in 1999
produced infected flower heads in 2000 and 2001, even though they were not
re-exposed to the fungus. It is unlikely that the Rudbeckia infections were the
result of spores released into the environment as other Rudbeckia plants
growing in the same area, but not directly infected with the fungus, never
produced visible infections. Moussonia deppeana (Schlechtend. et Cham.)
Hanst. infected with Fusarium moniliforma Sheldon, and Silene alba infected
with Ustilago violacea (Pers.) Roussel, both produced diseased flowers for up
to 4 years after initial infection (Baker 1947, Lara and Ornelas 2003). Fusarium
proliferatum (Matsushima) Nirenberg remains in the host plant and causes the
recurrence of leaf spots and shoot rot for a number of years after initial infection
(Uchida 2005). Thus, once a plant within a population is infected, the potential
110 Southeastern Naturalist Vol. 5, No. 1
for spread to other individuals increases. That plants may remain infected for a
number of years is also important in that it has been recommended that new
populations of R. auriculata be established on protected sites within its range
from seeds or plants collected from natural populations as a conservation
measure for this rare species (Diamond and Boyd 2004).
Because insect vectors spread this pathogen, insect behavior must be
considered when discussing epidemiology of the disease. It has been discovered
that in many cases the fungal agents influence the behavior of insect
visitors. In Vaccinium, the fungus Monilinia reflects ultraviolet light in the
same range as the floral calyces and produces a sugary reward that attracts the
same species that regularly serve as pollinators. The insects pick up spores
while feeding on the sugary solution and transmit the spores to uninfected
plants or plant parts (Batra and Batra 1985). Fungal pseudo-flowers of Arabis,
caused by the fungus Puccinia, share many of the same visitors that act as
pollinators for Anemone patens L., and may influence reproductive success of
that species (Roy 1996). In Silene alba, diseased flowers were preferred by
nocturnal visitors (Real et al. 1992, Roche 1993). In other cases, pollinators
have been shown to discriminate against flowers that are infected by fungus
(Jennersten 1988). Pfunder and Roy (2000) reported shorter visits by pollinators
to fungal pseudo-flowers in Euphorbia cyparissia. This appears to be the
case with the Fusarium infection in R. auriculata. The most common insect
visitor at this site was Andrena aliciae (Diamond and Boyd 2004). These bees
collect pollen from flowers to provision their nests, and are oligolectic on
flowers of various species of Asteraceae (LaBerge 1967). In the field, these
insects visited infected flowers less often and spent less time on them. However,
even though these insects appear to discriminate against fungal infected
flowers, they do make mistakes based upon field observation and the recovery
of fungal spores from their bodies. This, coupled with the fact that they are
specialists, allows for the fungus to be spread from flower to flower and plant to
plant within the Rudbeckia population. These bees also tend to maximize their
foraging efforts by visiting large displays of flowers and moving from the
closest head to the next on the same plant and not moving from plant to plant
rapidly. This behavior of the pollinator localizes the dispersal of the fungus into
a relatively small area as indicated by results of our dispersal experiments.
Clumped distributions of pollinator-dispersed fungal infections and slow rates
of spread of the fungal pathogen have also been reported in Silene alba (Real et
al. 1992) and Silene virginica (Antonovics et al. 1996).
Very little is known about fungal infections of native plants, other than a
few dramatic cases such as Silene and members of the Cruciferae. The available
literature is heavily weighted towards crop and ornamental species (Farr et al.
1989). This is the first report of a pathogen infecting R. auriculata, although
this rare species has been closely monitored for over 15 years (Diamond and
Boyd 2004). A Fusarium floral infection similar to the one reported here for R.
auriculata was observed on plants of Rudbeckia hirta L. var. pulcherrima
Farw. (Rudbeckia bicolor Nutt.) in Bullock County, AL, in 2002. Microscopic
examination of that fungus indicated it was slightly different from F.
2006 A.R. Diamond, Jr., H. El Mayas, and R.S. Boyd 111
semitectum isolated from R. auriculata. Whether this represents another similar
species of Fusarium or a species-specific host-race of F. semitectum is
unknown. More work is needed to asses the distribution of this fungal pathogen
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