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Rudbeckia auriculata Infected with a Pollen-mimic Fungus in Alabama
Alvin R. Diamond, Jr., Hanan El Mayas, and Robert S. Boyd

Southeastern Naturalist, Volume 5, Number 1 (2006): 103–112

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2006 SOUTHEASTERN NATURALIST 5(1):103–112 Rudbeckia auriculata Infected with a Pollen-mimic Fungus in Alabama 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. Introduction 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 - adiamond@troy.edu. 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. Results 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). Discussion 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. 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