Why Insects Aggregate And The Role Of Aggregation Pheromones
There are few things that I could find more awe inspiring than witnessing an aggregation of a hundred thousand monarch butterflies in one small area. The aggregation behavior of many insects is a fascinating occurrence. It does however raise ones curiosity, what is the function of this behavior?
In this paper I am going to try to shed some light onto that question. First, I will give a detailed overview of the aggregation behavior of three insects; the monarch butterfly (Danaus plexippus), the mountain pine beetle (Dendroctonus ponderosae), and the convergent lady bird beetle (Hippodamia convergens).
I will then present some of the current thoughts on why insects aggregate. From the use of aggregation as a defensive strategy to aggregation as a mating strategy. Finally, I will conclude with what the implication of this behavior is to man. For many insects this behavior could increase their chances of going extinct due to the destruction of their aggregating sites. Also understanding of this behavior in many pest insects could lead to a more environmentally safe way of managing them.
Many species of insects aggregate for various reasons. Some of these aggregations range from a few individuals and others to hundreds of thousands. This behavior is fascinating in itself. I am going to give specific examples of this behavior using the monarch butterfly (Danaus plexippus), mountain pine beetle (Dendroctunus ponderosae), and the convergent ladybird beetle (Hippodamia convergens).
The Monarch Butterfly
Every fall the monarch butterflies that range east of the Rockies migrate to one of about fifteen sites in inland Mexico, just south of the tropic of cancer (Masters et al. 1988). For many this migration requires them to travel a distance of up to 4500 km from their summer ranges. This migration takes place because the monarch is unable to withstand the harsh winters at Northern latitudes (Masters et al. 1988).
These sites are located on highly insulated Southwestern facing slopes in a mesic, oyamel fir (Abies relgiosa) forest ecosystem at a mean altitude of 3158 meters (Masters et al. 1988). The sites themselves range from 0.1 to 5.7 hectares with roughly 107 butterflies per hectare (Masters et al. 1988). These conditions apparently provide a suitable climate for them to overwinter in. The altitude and latitude results in a stable daily and seasonal temperature regime (Masters et al. 1988) It is thought that the monarch has been using the same overwintering sites since possibly the Pleistocene (Masters et al. 1988).
The monarchs reach the overwintering sites around November. Sites can contain from 50,000-200,000 individuals (Wells et al. 1990). Members of these aggregations survive on stored lipids, because food is rare (Wells et al. 1990). They are fairly inactive flying occasionally when disturbed or to drink water. Mating is also very rare in these populations (Masters et al. 1988; Wells et al. 1990).
The monarchs begin remigration to their summer ranges in the spring. The same butterflies do not return the following year. There are several spring and summer generations, before members of this species must return to these overwintering sites (Masters et al. 1988). It is important to note that there are other overwintering aggregation sites for the monarch in North America. Monarch s West of the Rockies aggregate in coastal California (Wells et al. 1988).
The Mountain Pine Beetle
The mountain pine beetle is an economically important pest of trees. In the larval and adult stages it can be found feeding on the inner bark of their preferred host lodgepole pine (Pinus contorta). They break diapause in the spring and emerge as adults. Males are believed to emerge first. This is thought to promote outbreeding (Borden 1982). After a short dispersal flight, they seek out new hosts. They prefer to attack trees that are physiologically weakened, diseased, or dead (Borden 1982).
The first beetle to discover a suitable host is called the pioneer beetle. After he decides a host is suitable, he will enter it and release an aggregation pheromone. This pheromone combined with natural odors of the host is very attractive to other mountain pine beetles. They use this odor trail to find the host. Once the host tree is colonized to the appropriate density and mating pairs are established an anti-aggregation pheromone is released (Borden 1982). This is done to ensure that they do not overuse the resource and have their offspring die due to a lack of food.
Convergent Ladybird Beetles
Hippodamia convergens has been found aggregating in many parts of the West on the shores of lakes and reservoirs (Lee 1980; Simpson and Welborn 1975). Other species such as Coccinella septmepuctata have been found in large aggregations in coastal areas such as Delaware (Schaefer et al. 1987). These aggregations occur in August, September and in the spring with the beetles gradually leaving the area after two to three weeks (Lee 1980, Schaefer et al. 1987).
What happens to the beetles between those months is unknown. There have been a few reports of findings of small aggregations (less than 150 individuals) beneath loose bark, and in wood crevices (Lee 1980). This phenomena has received little attention in the scientific literature (Lee 1980).
When aggregations are present several hundred to more than a thousand individuals can be collected in a fifteen to twenty minute time period (Lee 1980). The activity of H. convergens in these aggregations appears to be temperature related. If the beetles are disturbed on warm days they will move about rapidly or take flight. On cool days they respond by moving slowly or dropping to the ground (Lee 1980). During these aggregations the beetles copulate often, although no ovipositing females or larval ladybird beetles can be observed (Lee 1980). It is also believed that they do not feed while in these aggregations.
Comparative dissections of aggregating beetles, showed them to have empty stomachs as compared to the ones collected in corn fields during the summer which usually had aphid parts in them (Lee 1980). The beetles in these aggregations are characterized by the presence of a well developed fat body, a reduction in the size of the empty midgut, and a lack of ovigenesis (Lee 1980).
Why Do Insects Aggregate?
After examining the phenomena of insect aggregation it raises a question, why do they aggregate? What sort of advantage is conferred to them for participating in this behavior? What sort of selection pressure would choose for this trait?
In this section I am going to present some of the current thoughts on why some insects aggregate. I am going to specifically use the monarch butterfly, mountain pine beetle and convergent ladybird beetles as examples. As well as some other insects where applicable. This section will be presented in four subsections; environmental conditions, aggregation as a mating strategy, aggregation as a defensive strategy and chemical cues in aggregation.
Some insects such as the monarch inhabit Northern latitudes in the summer and are not capable of surviving in those areas during the winter (Masters et al. 1988). For this reason they must fly south to find conditions that are suitable for overwintering. If this is the case why must they aggregate in the same place? It is possible that they require a specific set of conditions that can only be met at the sites in Mexico. It has been determined that they are vulnerable to environmental constraints (Masters et al. 1988).
Body temperatures below -2 degrees Celsius begin killing monarchs and fifty percent die at -7.8 degrees Celsius (Masters et al. 1988). Also if temperatures become to high it may break the monarchs overwintering diapause and they may remigrate prematurely (Masters et al. 1988). So I would argue that it is possible that the monarchs aggregate in these areas because they need the correct environmental parameters which are met only at these sites in Mexico.
There are other insects whose movements may be related to environmental conditions. The convergent ladybird beetle and alfalfa weevil (Hypera postica) can often be found on the shores of lakes and reservoirs. It is thought that their movement to these areas may be based on their desire to seek areas of higher relative humidity (Simpson and Welborn 1975). Apparently H. convergens also requires free water to maintain a proper water balance (Simpson and Welborn 1975).
The alfalfa weevil has been shown to have a strong attraction to the increased humidity gradient produced by large volumes of water in the near proximity of alfalfa in semiarid regions (Simpson and Welborn 1975). So the cause of the aggregations in these two insect species may be motivated by the desire of the insect to be within preferable environmental conditions.
Aggregation As A Mating Strategy
For some species of Lepidoptera, aggregation has been theorized to be beneficial to the insect and in others it has been theorized to be a disadvantage. I am going to use the monarch butterfly to illustrate an example of a hypothesis that believes aggregation to be beneficial in mating. I will then use the Nymphalid butterfly Euphydryas anicia to illustrate an example of aggregating conferring a disadvantage in mating.
For the monarch, as it may already have become apparent, there may not be one simple inclusive reason for why they aggregate and what advantage it confers. As of yet there is no known reason for why aggregation has been selected for in the monarch (Wells et al. 1990). One theory that has been presented is that aggregation is beneficial for mating and providing an energy store for the female to remigrate on (Wells et al. 1990). This is thought to be a possible mechanism for selection because of how the monarch aggregations break up. At the beginning of spring as the monarchs began remigrating there is a mating frenzy.
The females mate with as many males as possible. Each time a female mates with a male, the male passes to the female and energy rich spermatophore. It is believed that the female tries to get as many of these spermataphores as possible to replenish her energy supply for the remigration (Wells et al. 1990). It is important to remember that they have been surviving on stored lipids during the winter so this added energy supply could be very important. It has been argued that these multiple matings, coupled with the nutrient absorption of the spermatophore by the female increases the monarchs fecundity (Wells et al. 1990). Multiple matings in such a short span of time would not be possible if the monarchs were not living in aggregations (Wells et al. 1990).
For the Nymphalid butterfly Euphydryas anicia it has been theorized that the hilltop aggregating behavior during mating season by the male may confer a disadvantage for participating males of this species (Odendall et al. 1988). It had once been thought that this behavior attracted females and conferred a mating advantage to the participating individuals (Odendall et al. 1988). The disadvantage is thought to be the result of the male searching behavior (Odendall et al. 1988).
Males of this species actively seek out females. Taking a closer look at anything that they might mistake for a female. Often times they mistake males for females and inadvertently waste their time chasing other males. In high population densities once there are a few males chasing each other, it attracts other males who are actively searching for females. This results in a bunch of males chasing each other around hoping the other to be a female. While the males that aren’t joining this aggregation are finding and mating with the females (Odendall et al. 1988).
Aggregation As a Defensive Strategy
Many aposematically colored insects aggregate. These are insects that have some form of chemical defense against predation and are usually brightly colored. Predators learn to avoid these insects after experiencing their unpleasant defense chemicals. The question that can then be asked is why do they aggregate? These insects being brightly colored and living in aggregations are very easy to detect. Much more so than an individual. It is believed that this behavior helps emphasize the insects warning coloration and also helps to dilute predation (Gagliardo and Guilford 1993; Sillen-Tullberg and Leimar 1988).
The hypothesis that aggregation functions directly to enhance the effectiveness of warning signals, or the chemical defenses on which they depend, by exploiting predator learning mechanism has been tested by Gagliardo and Guilford. This hypothesis was tested using domestic chicks. They were presented with food items of different colors. All of the food items of one certain color were sprayed with a solution of Quinine and mustard. The chicks where then tested on their ability to learn to avoid the unpalatable colored foods. It was found that they learned to avoid the distasteful food fastest if it was placed in an aggregation then if it were spread out (Gagliardo and Guilford 1993).
They also did not need to eat as many of the aggregating food items to learn to avoid them (Gagliardo and Guilford 1993). So it was the conclusion of this study that aggregation functions to enhance the warning signal that they are unpalatable (Galiardo and Guilford 1993).
A model was created by Sillen-Tullberg and Leimar on predator discovery and attack of aposematically colored insects. This model had a few basic assumptions it was based on. These assumptions help show why aggregation behavior may be advantageous for these insects. The first is that there is a dilution effect of predation in a group. If it is advantageous for an insect to be a member of an aggregation it has to decrease the chance of that individual being eaten when discovered by a predator (Sillen-Tullberg and Leimar 1988). Your neighbor might get eaten but chances are you won’t.
It is also believed that the selection pressures for these species should choose for an increase in aggregation size (Sillen-Tullberg and Leimar 1988). It has been shown for the monarch butterfly that the frequency of predation is inversely related to aggregation size (Sillen-Tullberg and Leimar 1988). By this they are saying that predation should be equal on a group no matter what the size. Therefore the larger the group the less that will be taken.
Aggregation Pheromones (Chemical Cues)
There are many species of insects that use chemicals to communicate. One of the common chemicals used in some insect species is an aggregation pheromone. This pheromone is a species specific chemical message that elicits aggregation.
I will give an example of the importance of this behavior using the mountain pine beetle. The mountain pine beetle after dispersing, searches for a suitable host in two ways. The first is to look for the correct cues emitted from the host or by following the scent trail of the aggregation pheromone emitted by another member of it s species that has already found a host.
It might be thought that this would not be productive for the beetle because then it would have to share his resource with others of it s species. It has been theorized that the beetles need to aggregate in sufficient numbers to overcome the host resistance, to utilize the host optimally, and establish themselves successfully so that they can rear their broods (Borden 1982). They also make sure to not overpopulate the resource by emitting an anti-aggregation pheromone once the appropriate number of beetles have established themselves in the tree.
The Implications of This Behavior To Us:
There are two major implications of this behavior to us. The first is that it may endanger some insects further existence on this planet. The other is that for many species of pest insects that aggregate, understanding of this behavior could lead to more environmentally safe control methods.
Insects such as the monarch butterfly that return to the same aggregation sites every year are threatened by destruction of their overwintering habitat. It has been hypothesized that the Eastern North American migratory phenomenon of the monarch is now threatened with extinction and will probably be destroyed within 10-20 years (Brower and Malcolm 1991). There are many other contributing factors to their predicted disappearance. They include things such as the spraying of Dipel (Baccilus thuringiensis) to control pest insects in the surrounding forest, increased tourism affecting surrounding vegetation, commercial logging, and slash and burn agriculture (Brower and Malcolm 1991).
The two biggest threats are the logging and the slash and burn agriculture. Even thinning of the monarchs overwintering habitat results in an increase of exposure to the environment (Masters et al. 1988). This destruction of their microhabitat speeds up nocturnal heat loss that increases freezing mortality (Brower and Malcolm 1991). Also the slash and burn agriculture in surrounding areas lets billows of smoke rise up the mountain through the monarchs aggregation. This smoke screen cause the monarchs to fly around. Any excessive flight activity will cause an increase in their lipid depletion which would result in a higher number of monarchs dying from starvation (Brower and Malcolm 1991).
Use of the aggregation behavior of some insects as a control measure could be a very effective means of control. Especially with those species that use aggregation pheromones. In the case of the mountain pine beetle, valuable stands of trees can be protected using the aggregation and anti-aggregation pheromone. By placing the aggregation pheromone in a non-valued stand of trees and placing the anti-aggregation pheromone in a valuable stand of trees you can attract the beetles away from a valued stand of trees (Lindgren and Borden 1993). Identification and understanding of the use of aggregation pheromones could prove to be invaluable for other insect pests as well.
It should now be apparent that the aggregation behavior of different insects is variable. The advantage that is being conferred is not always the same. It is somewhat surprising to see that this behavior has been well documented on some subjects, but not for all of them. I believe that research should continue to be conducted on this behavior for three reasons. The first is to satisfy our own curiosity. The second is to gain an understanding of what needs to be done to help preserve insects such as the monarch butterfly whose Eastern migratory phase is threatened with extinction. Finally, to help discover new ways to control pests that exhibit this behavior, without using insecticides.
- Borden JH (1982) Chapter 4 Aggregation Pheromone. Bark Beetles in North American Conifers. University of Texas Press, Austin.
- Brower LP, Malcolm SB (1991) Animal migrations: endangered phenomena. American Zoologist 31: 265-276.
- Gagliardo A, Guilford T (1993) Why do warning-colored prey live gregariously? Proceedings of the Royal Society of London B-Biological Sciences 251: 69-74
- Hochberg ME (1991) Viruses as costs to gregarious feeding behavior in the Lepidoptera. Oikos 61: 291-296
- Lee RE (1980) Aggregation of Lady Beetles on the Shores of Lakes. The American Midland Naturalist 104: 295-304
- Lindgren BS, Borden JH (1993) Displacement and aggregation of mountain pine beetles, Dendroctonus ponderosae, in response to their anti-aggregation and aggregation pheromone. Canadian Journal of Forest Research 23: 286-290
- Masters AR, Malcolm SB, Brower LP (1988) Monarch butterfly (Danaus plexippus) thermoregulatory behavior and adaptations for overwintering in Mexico. Ecology 69: 458-467
- Mattson DJ, Gillin CM, Benson SA, Knight RR (1991) Bear feeding activity at alpine insect aggregation sites in the Yellowstone ecosystem. Canadian Journal of Zoology 69: 2430-2435
- Odendaal FJ, Turchin P, Stermitz FR (1988) An incidental-effect hypothesis explaining aggregation of males in a population of Euphydras anicia. The American Naturalist 132: 735-749
- Peng C, Weiss MJ (1992) Evidence of an aggregation pheromone in the flea beetle, Phyllotreta cruciferae. Journal of Chemical Ecology 18: 875-884
- Schaefer PW, Dysart RJ, Specht HB (1987) North-American distribution of Coccinella septempunctata and its mass appearance in coastal Delaware. Environmental Entomology 16: 368-373
- Sillen-Tullberg B, Leimar O (1988) The evolution of gregariousness in distasteful insects as a defense against predators. The American Naturalist 132: 723-734
- Simpson RG, Welborn CE (1975) Aggregations of Alfalfa Weevils, Hypera postica, Convergent Lady Beetles, Hippodamia convergens, and other insects. Environmental Entomology 4: 193-194
- Wells H, Wells PH, Cook P (1990) The Importance of overwinter aggregation for reproductive success monarch butterflies (Danaus plexippus). Journal of Theoretical Biology 147: 115-131
- Wolda H (1988) Insect Seasonality: Why? Annual Review of Ecology and Systematics 19: 1-18