Fungi attack plants – insects respond!

As she was preparing to do her dissertation research on the interactions between the Asian chestnut gall wasp, the chestnut blight disease and the European chestnut, Pilar Fernandez-Conradi read a lot of papers about fungal-insect-plant interactions.  She was impressed by the diversity of outcomes that resulted when plants were attacked by both insects and fungi, and wondered whether there were any generalities to glean from these research findings. She asked two basic questions. First, if a plant is infected by a fungus, is it more or less likely to be attacked by insects than is an uninfected plant?  Second, does an insect that attacks a fungal-infected plant perform better or worse than it would have on an uninfected plant?

D. Kuriphilus+Gnomo

Three-way interaction between the chestnut tree, the chestnut gall wasp, and the fungus Gnomopsis castanea. Female wasps induce the plant to create galls, which house developing larvae. Green globular galls (with a hint of rose-color) have not been infected by a fungus, while the very dark tissue is the the remains of a gall that was attacked by the fungus. Credit: Pilar Fernandez-Conradi.

Fernandez-Conradi and her colleagues thought they were more likely to discover a negative effect of fungal infection on the preference and performance of herbivorous insects.  Several studies had shown that nutrient quantity and quality of host plants is reduced by fungal infection, so it makes sense that insects would avoid infected plants.  But the researchers also knew that fungal infection can, in some cases, actually increase the sugar concentration of some plants, so insects might prefer those plants and also develop more rapidly on them. In addition, fungal infection can induce chemical defenses in plants that might make them less palatable to insects, or alternatively, fungal infection could weaken plant defenses making them more palatable to attacking insects.

To resolve this conundrum, Fernandez-Conradi and her colleagues did a meta-analysis, of the existing literature, identifying 1113 case studies based on 101 papers.  To be considered in the meta-analysis, all of the studies had to meet the following criteria: (1) report insect preference or performance on fungal-infected vs. uninfected plants, (2) report the Genus or species of the plant, fungus and insect, (3) report the mean response and a measure of variation (standard error, standard deviation or variance). The measure of variation allows researchers to calculate the effect size, which calculates the strength of the relationship that is being explored. The researchers found that, in general, insects avoid and perform worse on infected plants than they do on uninfected plants.

Fernandez-conradi-myfig

Mean effect size of insect preference and performance (combined) in response to fungal infection infection.  Error bars are 95% confidence intervals (CIs).  In this graph, and the next two graphs as well, a solid data point indicates a statistically significant effect.  You can also visually test for statistical significance by noting that the error bar does not cross the dashed vertical line that represents no effect (at the 0.0 value). The negative value indicates that insects respond negatively to fungal infection.

Fernandez-Conradi and her colleagues then broke down the data to explore several questions in more detail. For example, they wondered if the type of fungus mattered.  For their meta-analysis, they considered three types of fungi with different lifestyles: (1) biotrophic pathogens that develop on and extract nutrients from living plant tissues, (2) necrotrophic pathogens that secrete enzymes that kill plant cells, so they can develop and feed on the dead tissue, and (3) endophytes that live inside living plant tissue without causing visible disease symptoms.

Fernandez-conradiFig1

Effect of fungus lifestyle on insect performance.  k = the number of studies.  Different letters to the right of CIs indicate significant differences among the variables (lifestyles).

The meta-analysis showed an important fungus-lifestyle effect (see the graph to your left).  Insect performance was strongly reduced in biotrophic pathogens and endophytes, but not in necrotrophic pathogens, where insect performance actually improved slightly (but not significantly). The researchers point out that biotrophic pathogens and endophytes both develop in living plant tissues, while necrotrophic pathogens release cell-wall degrading enzymes which can cause the plant to release sugars and other nutrients.  These nutrients obviously benefit the fungus, but can additionally benefit insects that feed on the plants.

To further explore this lifestyle effect, Fernandez-Conradi and her colleagues broke down insect response into performance and preference, focusing on chewing insects, for which there were the most data. Insects showed lower performance on and reduced preference (i.e. increased avoidance) for plants infected with biotrophic pathogens. They also performed equally poorly on endophyte-infected plants, but did not avoid endophyte-infected plants (see graph below). This was surprising since you would expect natural selection to favor insects that can choose the best plants to feed on. The problem for insects may be that endophytic infection is basically symptomless, so the insects may, in many cases, be unable to tell that the plant is infected, and likely to be less nutritionally rewarding.

Fernandez-conradiFig2

Effects of fungal infection on preference and performance of chewing insects.  k = the number of studies.  Different letters to the right of CIs indicate significant differences among the variables. Variables that share one letter have similar effect sizes. 

Many ecological studies deal with two interacting species: a predator and a prey, or a parasite and its host.  Fernandez-Conradi and her colleagues remind us that though two-species interactions are much easier to study, many important real-world interactions involve three or more species. Their meta-analysis highlights that plant infection by pathogenic and endophytic fungi reduces the performance and preference of insects that feed on these plants. But fungus lifestyle plays an important role, and may have different effects on performance and preference. Their meta-analysis also suggests other related avenues for research.  For example, how are plant-fungus-insect interactions modified by other species, such as viruses, bacteria and parasitoids (an animal that lives on or inside an insect, and feeds on its tissues)? Or, what are the underlying molecular (hormonal) mechanisms that determine the response of the plant to fungal infection, and to insect attack?  Finally, how does time influence both plant and insect response?  If a plant is recently infected by a fungus, does it have a different effect on insect performance and preference than does a plant that has suffered from chronic infection.  There are very few data on these (and other) questions, but they are more likely to get pursued now that some basic relationships have been uncovered.

note: the paper that describes this research is from the journal Ecology. The reference is Fernandez‐Conradi, P., Jactel, H., Robin, C., Tack, A.J. and Castagneyrol, B., 2018. Fungi reduce preference and performance of insect herbivores on challenged plants. Ecology, 99(2), pp.300-311. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.

Saguaro survival: establishing an icon

Having grown up in the New York metropolitan area, my only contact with the saguaro cactus, Carnegiea gigantea, was from several TV westerns, which dubiously placed these mammoth cacti in New Mexico, Texas and Colorado.  In fact, the saguaro is limited to the Sonoran Desert of northwestern Mexico, extreme southeast California and southern and central Arizona. You won’t find these cacti further north, because a freeze lasting more than 24 hours kills them.  I still remember my first real sighting of these cacti; I was amazed at how distinct they seemed in comparison to the other vegetation, and I delighted in their abundance.

Daniel Winkler - Saguaro Photo 1

Dense patch of saguaros. Credit: Daniel Winkler

Many others delight in their abundance as well.  The flowers, fruits and seeds feed many animals (including humans).  They were an important food for the Tohono O’odham and Pima Indians – eaten fresh or converted into numerous products including wine, juice, jam and syrup.

Daniel Winkler - Saguaro Photo 2

Large saguaro with many fruits emanating from the apex of its branches. Credit: Daniel Winkler

Woodpeckers and flickers excavate nests in the saguaro’s trunk, which are subsequently occupied by other animals such as snakes, arthropods and small mammals.

nesthole

Saguaro with nest cavity excavated near the top of its trunk. Credit: Daniel Winkler

Daniel Winkler also delighted in the saguaro’s awesomeness. As he describes “I fell in love with answering some basic ecology questions about the saguaro. I was surprised that scientists had been studying this wonderful plant for almost 100 years and there were still many basic questions about the species general biology and ecology that remained unanswered. Thus, I was hooked immediately and became obsessed with saguaro.”

Don Swann - Photo of D. Winkler with young saguaros

Daniel Winkler with young saguaros. Credit: Don Swann

Winkler and his colleagues wanted to know how moisture, temperature and habitat influence the establishment or survival of juvenile saguaro seedlings. Previous research had shown that saguaro height can be used to estimate saguaro age, given knowledge of previous rainfall in a particular area. So buoyed by an army of citizen scientists whom they recruited with the help of social media, student groups from schools and volunteers working at the Saguaro National Park, the research team estimated the age of every saguaro on 36 4-ha plots (1 ha = 10,000 m2).

Going into the study, the researchers knew that rainfall was a very important factor, with saguaros surviving better during wet periods.  But they also knew that historically, some areas located near each other showed different establishment trends, thus they suspected that other variables, particularly land use and other landscape factors, might be important.  They did their research in two different districts within the park: 21 plots in the Rincon Mountain District (RMD) on the east side of the park, and 15 plots in the Tucson Mountain District (TMD) to the west. They classified each plot as a particular habitat type based on slope, elevation and soil-type. Bajada was low elevation, flat and had gravelly porous soils.  Foothills were intermediate elevation and intermediate slope, while sloped habitats had highest elevation, steepest slope, and the coarsest rockiest soils.

Daniel Winkler - Saguaro Photo 4

Panoramic view of Saguaro National Park showing diversity of habitats. Credit: Daniel Winkler.

Winkler and his colleagues calculated the Palmer Drought Severity Index (PDSI) for the years 1950-2003. The PDSI quantifies the water balance between precipitation and evapotranspiration, taking into account not only rainfall but also other factors such as temperature and cloud cover.  The PDSI was estimated by assessing tree ring width for each year in nearby woodlands; wet conditions have wide tree rings (maximum PDSI value = +6), while dry years have narrow tree rings (minimum PDSI value = -6).

The researchers discovered a very strong association between the PDSI and seedling establishment. Low PDSI at the beginning and especially the end of the time frame was associated with low seedling establishment, while high PDSI (particularly in the 1980s was associated with high rates of seedling establishment (top graph below).  But other patterns emerged as well.  For example, establishment was higher in the TMD during the wettest years, but higher in the RMD during the most recent drought (bottom graph below).

WinklerFig1

Top. Total number of saguaros (left Y-axis) established per hectare from 1950-2003 in relation to PDSI (dashed line, right Y-axis). Bottom. Total number of saguaros established per hectare in the Tucson Mountain District (TMD – filled bars) and the Rincon Mountain District (RMD – open bars)  from 1950-2003 in relation to PDSI (dashed line, right Y-axis).

Saguaro establishment increased in all habitats when conditions were relatively wet (more positive PDSI values).  Under drought conditions, slopes had greatest saguaro establishment, while establishment increased more rapidly in foothills (and to a lesser extent in Bajadas) as moisture levels increased.

WinklerFig2

Model projecting number of saguaros established in the three major habitats in relation to PDSI.  Shaded regions are 95% confidence intervals.

The researchers were surprised at how tight the connection was between drought and saguaro establishment. But landscape features are also important.  The TMD is warmer and dryer than the nearby RMD, and had substantially lower establishment during the recent drought. The slopes in the RMD are steeper and rockier than sloped areas of the TMD, and may buffer saguaros from drought by capturing water in rock crevices and holding it for longer periods of time so it can be absorbed by saguaro roots. Nurse trees that provide shade to young saguaros may also be more common on the RMD slopes.

Winkler and his colleagues are concerned about the long-term impacts of climate change on saguaro populations, particularly in the drier areas of the TMD. They urge researchers to explore how long-term management of grazing and invasive species influences saguaro establishment across the landscape.  They also encourage researchers to gather some very basic data about saguaros, such as how they access water and how human water use patterns influence the water’s availability to this iconic species.

note: the paper that describes this research is from the journal Ecology. The reference is Winkler, D. E., Conver, J. L., Huxman, T. E. and Swann, D. E. (2018), The interaction of drought and habitat explain space–time patterns of establishment in saguaro (Carnegiea gigantea). Ecology 99: 621-631. doi:10.1002/ecy.2124. Thanks to the Ecological Society of America for allowing me to use figures from the paper. Copyright © 2018 by the Ecological Society of America. All rights reserved.