Ophryocystis elektroskirrha is an obligate, neogregarine protozoan parasite in the phylum Apicomplexa that infects monarch and queen butterflies. This parasite, shown above (green arrow), was first discovered infecting monarch and queen butterflies in Florida in the late 1960s (McLaughlin and Myers 1970). There are no known other hosts. It has since been found in all other monarch populations world-wide. Because of this world-wide range, all indications are that this parasite has coevolved with monarchs (i.e. it is a naturally occurring parasite).
Dormant spores of this parasite occur on the exterior of the cuticles of infected butterflies, sandwiched in between the butterfly's scales. When viewed under a light microscope at 40 to 100x, they appear as small, brown or black lemon-shaped objects about 1/100th the size of a butterfly scale as shown in the image above. Here is a picture of spores at 400X.
The images below (taken by Chip Taylor) show scanning electron micrographs of parasite spores clustered on abdominal scales from a parasitized monarch.
Life Cycle and Transmission
The life cycle of OE is closely related to the developmental cycle of its host. Parasites are vertically transmitted from females to their offspring when the females scatter dormant spores of this disease on milkweed during oviposition (Altizer et al. 2004). Spores are then eaten by larvae, germinate in gut, migrate to hypoderm, undergo 2 phases of vegetative reproduction. After the host pupates, the sexual phase of reproduction is initiated. About 3 days before the adults emerge, spores can be seen forming through the pupal integument. Infected adults emerge covered with spores, with the highest densities on their abdomens. Once hosts are infected, they do not recover. By the time adults emerge with parasite spores, all physical damage by the parasite has been done by this point The parasites do not continue replicating on adults, and these dormant spores on adult monarchs must be eaten by another larva to continue development. More details on the life cycle of OE are provided in McLaughlin and Myers (1970).
Detecting OE Infection
Pupae infected with OE show dark spots or blotches about 3 days before adult butterflies eclose. These are developing parasite spores, and lesions or ripples of many thousands of these spores can be seen through the pupal integument before any pigment is laid down on the butterfly scales. A monarch dissected from its pupal case at this stage will be covered with parasite spores (everything black in the image below aside from the background). Spores form on the eyes, antennae, wing veins, but by far the greatest number of spores form on the abdomen.
Because most parasite transmission was assumed to be maternal (from infected females to their offspring), people had speculated that this disease would not have large negative effects on host fitness (and would not be a concern for monarch populations), because the fitness of the parasite would hinge upon the reproductive output of infected females.
However, research has shown that adults that are severely infected with OE often have difficulty emerging from their pupal cases, and can be too weak to cling to their pupal case to fully expand their wings. These heavily infected adults either fail to eclose fully or fall to the ground, leading to severe wing deformities and relatively rapid death.
The abdominal cuticles of heavily infected adults are damaged by the large numbers of parasite spores that distrupt the integument (pictured below), and this causes the adults to lose weight at a faster rate than healthy individuals, especially if they do not have unlimited access to water or nectar (Altizer 2001).
Heavily infected adults can also be smaller than healthy butterflies, weigh less upon eclosion, and have a shortened adult lifespan. On the other hand, many parasitized monarchs do eclose normally, show no signs of deformity, and can be nearly impossible to distinguish from healthy butterflies without looking directly for the parasite spores. For more information on the effects of this parasite on the individual fitness of monarch butterflies, see Altizer and Oberhauser (1999) and Leong et al. (1997).
Sampling Monarchs for Parasites
Monarchs can be easily assessed for parasite loads by pressing a piece of ultraclear Scotch TM tape on their abdomens and counting the number of spores in a 1cm-2 area. This slide shows how spores appear relative to abdominal scales under the light microscope at 200x.
In our lab, we use this 'tape' method to categorize parasite loads on an approximate logarithmic scale of 0-5, with 5 being the most heavily infected class, and 0 being butterflies with no detectable spores. This method allows for rapid classification of disease status and the severity infection and is highly correlated with the log of total infection loads estimated using a destructive wash-and count method. For more information on how to test for OE parasites in monarch butterflies using the tape method click here. People in our lab have also developed more innovative methods for using digital image analyses to get more refined and continuous measures of spore densities (below) (Davis et al. 2004).
Digital picture of scales and spores obtained from an infected monarch. OE spores look like dust particles in this picture.
Same picture after digitally removing scales. Computer then does the rest. There are approximately 3600 spores in this picture!