A prominent winter feature of abandoned fields, right-of-ways, and city lots in temperate North America are the remains of the tall goldenrod (Solidago altissima).  Tall goldenrod is one of several herb species that form the pioneer communities of secondary succession, colonizing sites previously occupied by an ecological community.  It is not uncommon for goldenrod to be the dominant plant species in an old field.  Goldenrod has wide tolerance for variable soil and climatic conditions and therefore is found across much of North America.

Because this perennial herb possesses a substantial stem, the dead above-ground plant parts often remain above the snow as a visible part of the winter landscape. (The below-ground parts live to perenniate the individual plant the next season.)   In general, 20% to 30% of goldenrod plants have thick-walled stem swellings called galls in some fields, over half of the plants have stem galls, while none have them in other locations.

Because of the bad press, all of it misconceived, that goldenrod gets relative to hay fever, it is useful to here point out its innocence. Students conducting the activities naturally would be handling dried specimens that had been pollinated months earlier in late summer. Nonetheless, there may be some apprehension about the plant's supposed allergic properties. Goldenrod has been falsely blamed for causing allergic hay fever reactions because it occurs with ragweed in young fields. Ragweed, which is wind pollinated, is an excessive pollen producer and its airborne pollen causes hay fever. In contrast, goldenrod plants, with their bright yellow insect-attracting flowers, produce heavy sticky clumps of pollen which only rarely encounters the human nose, and do not result in allergies.

The Causes of Galls on Goldenrod Stems

Galls are abnormal plant tissue growths formed in response to an invading gall-making organism.  The stimulus may be mechanical or chemical; the organism may be a bacterium, fungus, nematode, mite or insect.  One view is that gall formation is not a defensive response by the plant, but rather a forced growth response governed by the invading parasite.  Goldenrod is invaded by more than 50 kinds of parasitic insects.  Galls can form on any part of the plant, although each kind of insect forms galls only on a specific part of the plant such as leaves, stem, or rhizome (underground stem).

Several insects cause galls to form on various portions of the goldenrod's stem.  This article focuses on two of the more common and widely distributed goldenrod stem galls, the ball gall, and the elliptical gall.  Each kind of stem gall is caused by a different insect species; while the ball gall-forming species predominates in most fields of goldenrod, the predominant species may vary from field to field.

Stem galls can form only within the meristem, the young undifferentiated (unspecialized) tissues located at the tip of the growing stem.  Gall makers cause the plant to alter the normal development of its tissues.  Normal cellular differentiation is inhibited, followed by cellular overproliferation (rapid growth of cells), abnormal cellular proliferation (production of cells that are different from normal cells of the stem), and redifferentiation of cells.  Thus the gall is a pathological structure to the plant, and the events that form it are reminiscent of cancer in animals.  The stem above the gall, however, continues its normal growth above the location of the gall.  The stem gall that eventually forms is of a different shape and character for each gall maker, because each gall-making species attacks a different goldenrod stem tissue.  Therefore, each gall-making species will have a different effect upon an individual plant.

The Life Cycle of Goldenrod Stem Gall Insects

Complete metamorphosis characterizes the life history pattern of the insects in the fly and moth families which cause goldenrod stem galls to form.  The egg hatches into a larva which feeds voraciously, and when mature, transforms into an inactive pupa from which the adult of the next generation emerges.  In the complete metamorphosis life history pattern, the larva is largely a feeding stage, whereas the adult is largely a reproductive stage.  The timing of each life history stage depends upon (1) the species of gall-forming insect, (2) the temperate zone latitude in which the gall-forming insect lives, and (3) the average temperature during the seasons of its development.  The time-of-year information for various life history events given in this account are generalizations from various sources.

Ball galls on goldenrod stems are caused by the gall fly (Eurosta solidaginis), a small fruit fly with banded wings.  The fruit fly family (Tephritidae) contains many species which cause severe agricultural damage; the apple maggot and Mediterranean fruit fly are well known, and unloved.  The goldenrod gall fly, a fruit fly that attacks stems not fruit, occurs widely from Nova Scotia to British Columbia and into southern United States, over the range of the tall goldenrod.

The gall fly's natural history has been described in detail in a classic paper by Uhler (1951), and is summarized in Figure 1.  In general, the adult fly emerges in spring (early May to mid June) and spends most of its life near the terminal buds of the Tall goldenrod plant.  An individual fly does not live long but can mate from its emergence until it dies some two weeks later.  Mating involves a courtship in which the pair performs an elaborate wing-vibrating "dance" prior to copulation.   After mating, the female injects an egg (oviposition) into the leaves that surround the terminal growing bud of the goldenrod plant.  The timing of oviposition corresponds to the maximum growth rate of the goldenrod plant, which also occurs between mid-May and late June.  The plants at this time are about 70 cm (2 ft) tall.

The gall fly egg hatches into a larva some 7-12 days later in mid-May to late June.  The newly hatched larva burrows a few millimeters into the goldenrod meristem.  A round gall, stimulated by larval secretions, becomes externally visible on the stem in about three weeks.  The larva spends the summer feeding on the gall's inner most nutritive layer. It is not uncommon for some stems to possess two, three, or even four galls.  At the end of the growing season, the mature gall is 10-30 mm in diameter and is 20-160 cm above ground.  The white larva, or maggot, spends the summer feeding with its mouth hooks, and growing inside the gall.  It reaches its peak barrel-shaped size in September.  At peak larval size, it digs an exit tunnel with its mouth parts, leaving a window of epidermal cells through which the adult fly will break in the spring.  Most exit tunnels are made in the upper half, or dome, of the gall (the lower half is the hold).

The fly spends the winter as a diapausing (inactive) larva within the gall.  The gall functions to protect the larva from direct sunlight, rain, snow, and ice. The spongy walls of the gall, however, are not sufficient to protect the larva from freezing to death during severe cold spells as it has no significant insulating properties.  The larva also makes antifreeze compounds in its tissues, and its body fluids become extensively supercooled prior to diapause. This prevents the formation of cell-destroying ice crystals during the winter months.

In the following spring (March-April), the inactive larva transforms into a pupa.  In a month or two, the short-lived adult emerges.  In order to emerge from the gall, the adult fly must crawl through the exit tunnel and break through the epidermal window.  As it does not have chewing mouth parts, it does this with a special structure on its forehead, the ptilinium.  After ramming through the epidermal window, this structure is useless to the fly and it is reabsorbed into its head.

Elliptical, or spindle, goldenrod galls are caused by the gall moth, Gnorimoschema gallaesolidaginis.  Gall moths overwinter as eggs on goldenrod plant litter on the ground under the snow.  Larvae hatch from the eggs in spring (May), locate a young goldenrod shoot and burrow through its meristem for 2-4 cm.  It is believed that gall formation is stimulated, at least in part, by the mechanical actions of the feeding of the moth larva.  The larva eats and grows within the gall until late July.  It then bores an exit hole in the upper parts of the gall and plugs it up with silk and plant material.  The exit hole tends to face north more frequently than south.  The larva probably follows the path of least resistance in boring its exit hole; the cells on the north side of the plant are usually larger because they receive less sunlight and may be easier to bore through.  The moth larva then pupates for 35-45 days in mid summer.  In the fall (September), the adult moth emerges, mates, and lays eggs on the lower stem and leaves of the goldenrod plant, initiating the life cycle all over again.  Note that elliptical galls examined in winter never contain its maker, although it may contain the larva or pupa of another insect.

Effect of Galls on Goldenrod Plants

Most investigators agree that the gall insect-plant association is parasitic.  The gall-forming insects are herbivorous parasites on the goldenrod plant, gaining shelter, protection from enemies, and a continuous reliable source of nourishment from the gall.  In this parasitic relationship, the gall insect gains resources from the plant while the plant is harmed.

In what ways is the plant harmed by the relationship?  One way to investigate this problem is to consider the allocation of resources by an organism.  Any organism has a fixed amount of resources which it can use for either growth, maintenance, or reproduction.  The proportion of energy it allocates to each function depends upon how the organism has adapted to its ecological niche.  For example, late successional plants such as trees, in general, allocate more of their energy to maintenance and less to reproduction.  In contrast, early successional herbs, such as goldenrod, use a higher proportion of their energy for growth and reproduction, and less for maintenance.  Parasites may significantly affect how a host organism's energy is allocated.

The presence of a stem gall on a goldenrod plant does not have an obvious adverse effect upon the goldenrod plant.  For example, Uhler (1951) found no difference in height between plants with and without galls.  In a recent study the stem heights of plants with galls did not differ significantly from ungalled plants at any time during the growing season.  However, the presence of a stem gall can have several important effects upon the reproductive capacity of the host goldenrod plant.  Recent evidence of Hartnett & Abrahamson (1979) indicates that the presence of either kind of gall can alter resource allocation in tall goldenrod in several ways:  (1) it causes a decrease in the amount of energy allocated to flowering, and (2) it causes goldenrod to allocate less energy to reproduction by producing fewer, smaller seeds.  Since established populations of goldenrod reproduce nearly entirely by vegetative means from the rhizome or underground stem, the following year's population size on an established site would be affected because the gall maker attack in one season reduces the number of new rhizomes, and hence new ramets (stems) in the following season. Plants bearing ball galls produce fewer rhizomes than non-gall bearing ones.  Thus, the ability of parasitized plants to reproduce vegetatively in the following year is impaired and their ability to colonize new sites is reduced because they bear fewer, smaller seeds.  Hartnett and Abrahamson (1979) point out that the alteration in the plant's resource allocation could be an adaptive response of the plant to the galls, or, the immediate direct effect of the gall insect's activity.  In any event, the parasitic gall maker can have a significant negative effect upon the fitness of its host plant, and, in turn, on the evolution of the plant's reproductive strategy.

Consumer Classification

Producers are organisms that transform energy, nearly always sunlight, into a form which can be used by other organisms, the consumers.  It is a rule of ecology that energy in ecosystems flows from producers (usually plants) to consumers (usually animals).  This flow of energy can be described by means of food web diagrams:

 Predators are one kind of consumer.  Predation is the consumption of one organism, the prey, by another, the predator, while the former is still living. This broad definition includes many kinds of feeding relationships and many kinds of predators, including parasites.  (Other consumers are detritivores, organisms which receive energy from dead materials.)

Predators may be classed "taxonomically" as carnivores (meat eaters), herbivores (plant eaters), and omnivores which eat both animals and plants.  This classification helps identify what the predator's source of energy is.  Predators may also be classified on the basis of how they obtain their energy, a functional classification.  Functionally, there are four kinds of predators:  true predators, grazers, parasites, and parasitoids.  No matter what the functional classification, the predator always benefits and the prey is always harmed by the interaction.

True predators kill their prey immediately, and over their lifetime kill several or many prey individuals.  They may consume the entire prey or only parts of it.  Most true predators have broad diets, eating a variety of prey kinds, although examples of true predators which specialize on one kind of prey do exist.  The ambush bug hiding within the goldenrod flower head in the summer is a true predator; so are preying mantids, downy woodpeckers, weasels, chipmunks and squirrels.

Grazers are similar to true predators in that they feed on many different prey organism over their lifetime.  They differ from true predators in that they consume only part of each prey, and, although the effect may be harmful to the prey, it is rarely fatal.  Deer and sheep are familiar examples of grazers, as are leeches and mosquitoes.

Parasites are similar to grazers in consuming only a part of their host.  Like grazers their attacks are harmful to the host, but not usually fatal.  Parasites differ from grazers in that they attack only one or few individuals over their lifetime.  As a result, there evolves an intimate association between the parasite and its host, unlike grazers or true predators.  Many parasite species, thus, have evolved to infest only one or a few specific host species.  Examples of such parasites include the goldenrod gall moth and gall fly, which infest only the tall goldenrod or closely related species, as well as the more familiar tapeworms and liver flukes.

Although parasitoids are a functional class of predators known only from two insect orders, the Hymenoptera (wasps, bees, and ants) and the Diptera (flies), it has been estimated that the parasitoid feeding strategy is used by about 25% of all known insect species.  The adult parasitoid lays its eggs in, on or near its specific host, usually another arthropod.  The parasitoid larva that hatches does not immediately harm its host, but lives within it feeding on the latter`s tissues.  The host is eventually killed by the parasitoid larva, often prior to the host's pupation.  Thus, the parasitoid mode of feeding lies between that of a true predator and parasite.  Like a parasite, a parasitoid species nearly always specializes to feed on one individual of a specific host species; like a true predator, however, the host is always killed.  While parasites grow and may reproduce several generations within an unlimited food resource, parasitoids grow and reproduce one generation within a finite resource.  However, the effect of parasitoidism upon the host is identical to true predation, except it takes longer for the prey to die.

Predation on Parasitic Gall Flies

Not all gall fly pupae emerge the following year as adults: there is often high mortality due to predation by their many enemies.  For example, the larval and pupal stages of the gall fly are eaten by the larvae of two species of wasps.  In some goldenrod fields, the wasps cause 95% mortality of the gall fly and in other fields much less; the degree of wasp predation also varies from year to year within a particular field.  The wasps tend to attack the smaller ball galls because the shortness of their ovipositor limits their ability to reach into the central gall cavity to deposit an egg.  The gall fly is also occasionally preyed upon by a beetle, Mordellistena unicolor, and by two species of birds.

The principal wasp predator, Eurytoma obtusiventris, usually lays its eggs on the gall fly larva before the gall is formed.  The wasp larva causes its host to pupate early (by mid-August), and then feeds on the tissues of the pupa through the winter, inside the empty pupal case (puparium).  In winter, the presence of E. obtusiventris can be recognized within the gall by a brown pupal case considerably smaller than that of a normal gall fly, an associated "varnish-like" coating of the gall cavity, and the absence of an exit tunnel.

The second predatory wasp, Eurytoma gigantea, deposits its eggs inside the cavity of the developing gall.  After hatching, the wasp larva feeds externally on the fly larva and by late summer (end of August) has consumed it.  After eating the gall fly larva, the wasp larva feeds on the gall tissues, leaving black fecal pellets in a greatly enlarged central cavity.  E. gigantea spends the winter in the enlarged central cavity of the gall, pupates in June, and emerges as an adult in early to mid-July.  In winter, the presence of E. gigantea in a gall may be recognized by a vastly enlarged gall chamber without an exit tunnel, which is usually filled with black pellets.

Both wasp species are properly referred to as parasitoids, but their effect on the gall fly prey (or host) is identical to true predation.  In the student activities, the gall fly larvae are considered parasites on the goldenrod plants.  The wasps, in turn, are considered predators of the gall fly larvae.  In this way, we avoid introducing unnecessary new vocabulary, yet distinguish between the gall fly and wasp feeding strategy.  You may wish to point out the distinction between true predators and parasitoids to advanced placement students.   

The long thin larva of Mordellistena unicolor, a member of the flower beetle family (Mordellidae), is occasionally found in ball galls.  The mordellid beetle larva ordinarily lives inside a shallow tunnel which it constructs in the outer tissues of the gall.  The beetle is described by some investigators as an accidental predator upon the gall fly.  In many instances, near the end of the growing season, it tunnels through to the central gall chamber, where it consumes the gall fly larva or its wasp predator, and then itself pupates within the gall.  Other investigators describe the beetle as an inquiline, an occasional visitor, living side by side with the gall fly larva and causing no harm.  Presumably the beetle finds the gall a suitably sheltered place in which to feed, grow, and pupate, as do other occasional inhabitants of empty galls such as ants, spiders, millipedes, beetles, bees and thrips. 

The two wasp parasitoids and the beetle predator may be considered a parasitoid/predator guild for the gall fly.  A guild is a group of taxonomically unrelated species that feed on the same kind of environmental resource in a similar way.  This term describes groups of species that have very similar functions within an ecological community.

The elliptical gall moth guild is comprised of different wasp parasitoids than those that infest the gall fly, and, since the gall making moth is never found within its gall in the winter, any pupa or larva found in the winter within the moth gall must be one of the wasp parasitoids.  Gall moth larvae are so commonly attacked by many kinds of parasitoid species that few survive to become adults.  One common parasitoid is Calliephialtes notandus, which belongs to the Ichneumonidae wasp family.  Ichneumonid females are characterized by possessing a long ovipositor (egg depositor).  This wasp inserts its ovipositor into the gall and lays an egg on the moth larva.  Upon hatching, the wasp larva feeds within the moth larva and spins a brown silken cocoon in which it pupates; it emerges as an adult wasp in late summer.  Another wasp, Copidosoma gelechiae, lays an egg within the egg of the gall moth in the autumn.  This egg hatches within the developing moth larva, the resulting parasitoid larva feeding within the moth larva host.  The gall moth larva, however, continues to develop normally until pupation and only then dies.  Meanwhile, the wasp parasitoid has itself pupated within the moth larva and will emerge in late summer.  Three other wasp parasitoids belong to the gall moth-feeding guild, Eurytoma bolteri, Microgaster gelechiae, and Campoplex depressus.

Predators tend to congregate where there is a high density of prey.  Fields with higher densities of Tall goldenrod tend to have higher densities of both the elliptical and ball galls.  In turn, the higher the gall densities in a goldenrod field, the higher the densities of parasitoid predators.

Finally, the parasitic and predatory inhabitants of the various galls may fall prey to vertebrates -- an occasional mouse or squirrel, but more likely downy woodpeckers and black-capped chickadees.  These birds seem to prey upon the galls mainly in December - February when other food resources are unavailable.  The attacks of each of these birds may be recognized as follows: (1) deep narrow holes 1.2 - 1.5 cm deep are the work of downy woodpeckers, (2) large irregular holes are attributable to chickadees, and (3) surface scores to either.  Downy woodpeckers feed on the galls most heavily near the field edge, whereas chickadees feed on galls more uniformly throughout the field.  Both species reject abnormal or small galls as well as galls containing mordellid beetles.  They tend not to consume the obtuse wasp larvae suggested that the varnish-like wall coating associated with this parasitoid may be distasteful to birds.  Furthermore, birds prefer to feed upon multiple galls, galls which are higher above ground, and galls with live larvae within them.  While wasp predators tend to attack the smaller galls, birds feed on those of larger than average diameter.  Finally, these investigators claim that birds excavate the galls through the escape tunnel "much more often than can be attributed to chance".  They do not, however, provide data in support of this contention.

Beneath the surface of what appears to be simple relationships between organisms is the reality of a community of species interacting in complex ways.  In summary, one may describe the flow of energy in this community by the following food web diagram:

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