Monarchs, milkweeds and O. e.: It’s time for a more holistic approach

There have been many papers written on the relationship between monarchs and their neogregarine parasite Ophryocystis elektroscirrha, hereafter referred to as O.e. These papers have covered a number of topics including, infection rates, how spores are distributed by infected adults, how the relative attractiveness and overwintering persistence of tropical milkweed appears to contribute to the frequency of O.e., the relationship of sublethal infections on the fitness of monarchs, especially as it determines the ability to migrate, and frequency as it relates to continuous breeding and geographic distributions and others. These studies constitute a useful baseline or foundation for further studies. In this short article, I’m going to argue that to fully understand the relationship between monarchs and O.e. we need a more comprehensive approach, one that accounts for the seasonal and geographic dynamics of the monarch population, the density and frequency dependent interactions in the system, the impacts of other predators and parasites and the effects of weather on the outcomes. While I’m advocating a holistic approach, I’m not attacking the research conducted to date nor am I claiming to have the answers. However, I do feel that a broader understanding of the complexities of the interactions in monarchs’ annual cycle and its interactions with all components in the system will be helpful. There are some obvious relationships that are begging for data.

O.e. has a unique life-history that involves ingestion of spores by larvae but ends with masses of spores on the outside of the adult host. Here is the short version of that process. To become infected, a monarch larva consumes the chorion (egg shell) along with O.e. spores shed on the egg or the surrounding leaf surface during oviposition. A larva can also eat spores deposited on milkweed leaves by infected or contaminated monarchs that have landed on the leaves. The spores consumed by the caterpillar “germinate” in its alkaline gut and a malaria-like stage of O.e. (sporozoite) migrates through the gut wall to the tissues (hypoderm) beneath the caterpillar’s skin. This stage is followed by vegetative reproduction and then a period of quiescence. Late in the pupal stage, variously said to be the 8th day of pupation or three days before emergence, O.e. goes through a process of reproduction that results in a massive production of spores (sporulation) just beneath the cuticle of the pupa and on the outside of the developing monarch. Upon emergence, the adult monarch can carry extremely large numbers of spores, especially on the abdomen. The dust-like spores are lost progressively through the life of an infected adult monarch. O.e frequency is usually determined from sticky taped samples of scales taken from a monarch’s abdomen. Upon inspection with a microscope, high numbers (thousands) of spores indicate infection, low numbers (a hundred or less) indicate contamination through contact with other monarchs or contaminated surfaces. In the wild, an unknown portion of O.e. infected larvae, pupae and adults with crumpled wings die before they are able to take flight to reproduce or migrate, and therefore are not included in the sampling to determine the frequency of O.e. Thus, it’s likely that the mortality and morbidity due to O.e. is greater than measured. This mortality can be seen in badly infected monarch cultures, but we have no idea how common it is in the wild.

I’m going to start with migratory culling and how that relates to the carryover of O.e. spores from one year to the next. While it’s clear that a significant proportion of the infected monarchs are eliminated during the migration due to reduced life span and flight capability, there is no data indicating that infected monarchs return in the spring to establish the O.e. infection rate. If we assume that the culling eliminates nearly all of the highly infected individuals either during the migration, through the winter or during the migration from the overwintering sites to Texas, that means that O.e predominantly starts the next year as incidental spores carried on non-infected individuals (also referred to as contaminated or spore infested) through horizontal transfer due to contact with other individuals or contaminated surfaces. The proportion of returning monarchs that are contaminated with O.e. spores as they reach Texas is unknown. That proportion and how it varies from year to year is critical to our understanding of how O.e. increases each year. On the other hand, if a substantial number of infected females survive the migrations and reach Texas in the spring, the distribution of spores on the eggs they lay, and the milkweeds they contact, would result in a more efficient way to establish O.e.

The next consideration is how those spores are distributed on milkweeds as these returning monarchs move northward. The returning monarchs carrying spores advance at a rate of 30-55miles per day with some mating and with females laying eggs as they move northward. As this population progresses, the spores are dispersed on the milkweed foliage through egg laying and other foliage due to nectaring and resting. In effect, there is a trail of spores which thins out with increasing latitude to the point at the northern limit reached by overwintered monarchs where there are almost no spores to be ingested by monarch larvae. In other words, the loss of spores fits a decay function, i.e., a frequency of spores that declines with distance. In this scenario, relatively few of the first-generation monarch larvae will ingest spores and most of those larvae that do so will originate from the most southern range with milkweeds. However, we need to consider “egg dumping”. This term refers to the tendency of female monarchs, either the same female, or multiple females, to lay multiple eggs on relatively scarce new milkweed shoots. This concentration of egg laying and multiple touches by contaminated females is likely to have the effect of increasing the numbers of infected first-generation adults. Since egg dumping is usually reported only when milkweed shoots, or even mature plants, are scarce, this dynamic illustrates one of the frequency/density relationships in the system. If the abundance of O.e. contaminated females is high relative to the number of available shoots or mature plants, that favors multiple touches and multiple deposits of spores (frequency) along with eggs on relatively small numbers (density) of plants. That will certainly lead to an increase in O.e. What we don’t know is how much egg dumping occurs, how it differs regionally and from year to year. It seems likely that since we know that milkweeds are less abundant in some regions, such as the SE, that egg dumping is more common in that region. On the other hand, there is variation in the phenology of both milkweed growth and monarch occurrence such that, in some years, if milkweeds have emerged in abundance before the arrival of monarchs, the dumping will be less common resulting in lower rates of infection than in years when shoots are scarce. These dynamics could result in significantly different proportions of infected first-generation monarchs moving north from different regions as well as in different years. As monarchs continue to move north in May and early June, egg dumping is less of a factor since milkweeds have typically emerged and are abundant N of 40N at this time.

First generation monarchs begin moving N in the last week of April and they too, as a population, will leave a trail of spores which will also decline due to distance. It follows that relatively few of the monarchs reaching the latitudes N of 40N, but especially above 45N, will carry spores to the most northern and eastern latitudes and longitudes. Given what is known of migratory culling, it is likely that most of the spore-carrying first generation monarchs moving north will be either lightly infected or simply contaminated with spores through horizontal transfer.

How the O.e. numbers build up after the recolonization has occurred will depend on a number of factors starting with the number of recolonizing monarchs and the proportion carrying spore loads. Beyond that, we have to be concerned about the abundance and spatial distribution of milkweeds. These considerations take us back to the density and frequency-dependent relationships that determine the infection rate for the next generation. If there are low numbers of infected and contaminated individuals and milkweeds are exceedingly abundant relative to the monarch numbers, the infection rate for the next generation might increase slightly but will still be low. On the other hand, if the numbers of infected and contaminated females are high relative to the abundance of milkweeds, the frequency of O. e. will increase significantly. In highly fragmented environments where the distances between patches are substantial, there will be hot spots where the incidence of O.e. will be quite high if infected and contaminated females continue to return to the same plants for oviposition. Since there are few regions with an even distribution of milkweeds, it is likely that a fine-grained approach to sampling will find that Oe varies within regions as a function of monarch abundance as well as the spatial distribution and abundance of milkweeds.

The escape hypothesis, which posits that monarchs disperse to escape high frequency infection rates by O.e., doesn’t really fit with the monarchs’ seasonal migrations. In the spring, monarchs returning from Mexico simply migrate – distributing eggs (progeny) as the migration advances. They are not escaping a high incidence of O.e. That can also be said of the first- generation monarchs that migrate north from late April to early June. These monarchs are advancing into areas where milkweed is more abundant and where temperature and moisture conditions are more favorable for reproduction. If anything, monarchs are abandoning the southern latitudes due to the tendency for two of the more common milkweeds to senesce during the summer months and for high temperatures to be less favorable for reproduction. Further, once the migration stops at each latitude in June, monarchs disperse locally in search of milkweeds. Thereafter, the buildup of O. e. is a function of the size of the next generation, number of generations, abundance and distribution of milkweeds, interactions with predators and parasites that eliminate infected larvae and the weather. In effect, once the migration has stopped, the monarchs are stuck in one place irrespective of the buildup of O.e. or predators and parasites. One could argue that, if selection had favored escape from O.e., that the first-generation monarchs would not stop migrating across the latitudes through May and early June (See the puzzle solution –). The escape hypothesis seems to suggest that monarchs are aware of the O.e. infection rate or the buildup of predators and parasites. Cognition in insects? No, I don’t think so. It seems far more likely that dispersal and migration by monarchs is a selective response to changes in habitat quality.

In terms of the seasonal breeding dynamic, there is very little continuous reproduction south of 35N from late May until August. That’s related to the fact that, in much of the south, milkweeds senesce during the summer, and it is simply too hot for sustained reproduction. From that perspective, monarchs have been selected to vacate degrading habitats. That said, there are some exceptions where reproduction is continuous in coastal cities with lots of planted milkweed such as Houston and New Orleans. Based on that observation, and on the behavior of monarchs in areas such as southern Florida where reproduction is continuous, it seems that monarchs respond to the availability of resources rather than O.e., as well as other parasites and predators that are also common in those areas. O.e. infection rates are known to be high in these areas yet there appears to be no “escape”.

There is also the mid-summer migration in which monarchs move south of 40N to recolonize the southern latitudes from late July through the first three weeks of August. Some are probably carrying spores S from the northern latitudes. These monarchs are not “escaping” from areas with high frequencies of O.e. any more than the first gen monarchs are as they move N.

Because we can test for it, and determine its frequency, O. e. inspires concerns about the degree to which this parasite depresses the monarch population. Similar concerns have been voiced about the impact of introduced fire and crazy ants, ladybird beetles, European paper wasps and tachinid flies on monarch numbers. And then there are the periodic increases of resident parasites and predators that also take a toll. All of these species surely have an impact on monarch numbers, but to put these losses into context, we have to know where and when in the season these impacts occur. And in the case of monarchs that migrate, we have to know whether monarchs from all reaches of the eastern population have equal or strongly different probabilities of overwintering in Mexico and contributing to the population the following spring.

Lastly, O.e. appears to be a “self-limiting” disease/infection/organism. That is, a species that is capable of reducing the population of a host to a relatively low level from which, in time, the population will recover. In other words, monarchs and O.e. will cycle because of the spatial and temporal complexity of the environment. That complexity is related to the seasonal and spatial distribution of milkweeds and the presence of other species and weather conditions. There are a large number of parasites and predators that prey on monarch eggs, larvae and pupae such that the percentages reaching the adult stage are estimated to be 1-3%. As these species prey on monarchs, they also eliminate O.e. infected immatures. In some cases, the mortality rate due to these species approaches 100%. By eliminating adult monarchs and therefore reducing the distribution of spores to milkweed leaves and giving time for the O.e. spores that are present to degrade, portions of the larger range become monarch and O.e. free, allowing recovery when these locations are found by females that don’t carry spores. These actions create the complexity and escape in space monarchs need to recover from high levels of infection that reduce the population in other locations. Again, in these cases, the “escape” is simply an artifact of the constant dispersal conducted by monarch females in search of host plants. Fundamentally, there is nothing unique here since this dynamic is common to a large number of interactions between hosts and the species that prey on them. These dynamics are similar to those illustrated by a series of predator/prey and parasite/prey experiments conducted in greenhouses decades ago. In those experiments, predators or parasites could eliminate a host and themselves in the simplest of habitats. Complexity often produced cycles of hosts and parasites since the diversity/complexity of the habitats afforded escape by the hosts in time and space. Most greenhouse managers are well aware of the complexities involved in trying to control greenhouse pests with predators or parasites. Success is often temporary due to the ability of the prey (pest) species to escape in time and space.

Many of the hypothetical deductive scenarios I have outlined can be tested experimentally or, in some cases, through sampling that follows rigid protocols.

Conclusions

To understand the relationship between O.e., monarchs, milkweeds, predators, parasites and weather, we have to lay a foundation for the annual cycle of both monarchs and O.e as well as the seasonal, local and regional dynamics of the other species that interact with monarchs in a manner that modifies the O.e. frequency. In addition, we need to understand the density and frequency dependent interactions between monarchs, milkweeds and O.e. At present, our understanding of passive/horizontal transfer of O.e. spores is limited, and knowledge of the conditions, such as UV and high temperatures, that result in the degradation of O.e. spores is lacking. These conditions could explain the relatively low incidence of O. e. in Arizona in spite of the relatively low and highly fragmented distribution of milkweeds in much of that state.

Looking forward, in coming years, the continuing loss of grasslands, along with land conversion associated with development, will result in a loss of milkweeds, an increase in fragmentation and an increase in O.e. It should be noted that the recent increase in O. e. followed the adoption of herbicide tolerant crop lines in the early 2000s and the later adoption of the renewable fuel standard in late 2007 both of which resulted massive losses of milkweeds. These losses and the resulting increase in fragmentation could well account for the increase in O.e since the early 2000s. References to habitat losses due to these factors can be found in previous posts to this Blog.

Recent publications

Majewska, A. A., Davis,A. K., Altizer, S. and Jacobus C. de Roode. 2022. Parasite dynamics in North American monarchs predicted by host density and seasonal migratory culling. Journal of Animal Ecology.

Dargent, F., Gilmour, S. M., Brown, E. M., Kassen, R., and Heather M. Kharouba. 2021. Low prevalence of the parasite Ophryocystis elektroscirrha at the range edge of the eastern North American monarch (Danaus plexippus) butterfly population. Can. J. Zool. 99: 409–413.