Insect Outbreaks Revisited

Pedro Barbosa, Deborah K. Letourneau, Anurag A. Agrawal, Pedro Barbosa, Deborah K. Letourneau, Anurag A. Agrawal

• Publisher: Wiley-Blackwell
• Year: 2012
• Print ISBN: 9781444337594
• eBook ISBN: 9781118253847
• Edition: 1
• Topic: Biological Sciences
• Subtopic: Entomology
• Index: Biological Sciences

The abundance of insects can change dramatically from generation to generation; these generational changes may occur within a growing season or over a period of years. Such extraordinary density changes or "outbreaks" may be abrupt and ostensibly random, or population peaks may occur in a more or less cyclic fashion. They can be hugely destructive when the insect is a crop pest or carries diseases of humans, farm animals, or wildlife. Knowledge of these types of population dynamics and computer models that may help predict when they occur are very important.

This important new book revisits a subject not thoroughly discussed in such a publication since 1988 and brings an international scale to the issue of insect outbreaks.

Insect Outbreaks Revisited is intended for senior undergraduate and graduate students in ecology, population biology and entomology, as well as government and industry scientists doing research on pests, land managers, pest management personnel, extension personnel, conservation biologists and ecologists, and state, county and district foresters.

Part I

Physiological and Life History Perspectives

1

Insect Herbivore Outbreaks Viewed through a Physiological Framework: Insights from Orthoptera

Spencer T. Behmer and Anthony Joern

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1.1 Introduction

1.2 Which conditions favor the individual, and can lead to insect herbivore outbreaks?

1.2.1 Factors that influence performance in immature stages

1.2.2 Factors that influence performance in the adult stage

1.2.3 What happens to the individual as population density increases?

1.2.4 Density effects on group behavior

1.2.5 Population responses by insect herbivores to variably abundant nutritional resources

1.3 The plant-stress paradigm

1.4 Insect herbivore outbreaks – where do we go from here?

Acknowledgments

References

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For they covered the face of the whole earth, so that the land was darkened; and they did eat every herb of the land, and all the fruit of the trees which the hail had left: and there remained not any green thing in the trees, or in the herbs of the field, through all the land of Egypt.

Exodus 10:15 (King James Version)

The Cloud was hailing grasshoppers. The cloud was grasshoppers. Their bodies hid the sun and made darkness. Their thin, large wings gleamed and glittered. The rasping whirring of their wings filled the whole air and they hit the ground and the house with the noise of a hailstorm.

On the Banks of Plum Creek (by Laura Ingalls Wilder)

1.1 Introduction

Insect herbivore outbreaks, particularly orthopteran outbreaks, have plagued humans throughout recorded history. The Egyptian locust swarm described in the Old Testament is perhaps the most famous orthopteran outbreak story. Two species, the African desert locust (Schistocerca gregaria Forskål) and the migratory locust (Locusta migratoria (Linnaeus)), still outbreak regularly throughout large expanses of Africa and the Middle East. The most likely villain in the biblical swarm was the African desert locust, based on the broad array of the food plants described in the story. In contrast to the desert locust, the migratory locust is a specialist that feeds only on grasses. However, despite its restricted diet, the migratory locust has a larger geographic range, extending from all of northern and central Africa across to eastern China. It too has greatly impacted human society throughout historical time, especially in China. Parenthetically, the Chinese character for locust is composed of two parts, insect (虫) and emperor (皇); this character combination indicates the power of locusts – it was an insect capable of threatening an emperor’s supremacy. In China’s 5000-year history, 842 locust plagues have been recorded, with the earliest ones being described in the Book of Songs (770–476 BCE). How locust outbreaks endangered regimes and changed the destiny of China is also described in two other important ancient Chinese books – Zizhi Tongjian (which covers Chinese history from 403 BCE to 959 CE, including 16 dynasties) and Ch’ien Han Shu (which covers Chinese history from 206 BCE to 25 CE).

Although the recorded histories of Australia and the Americas are more recent, orthopteran outbreaks have a long history on these continents as well. The first recorded outbreak of the Australian plague locust (Chortoicetes terminifera (Walker)) was in 1844, followed by outbreaks from the 1870s onward (including multiple outbreaks in the early 2000s, most of which were controlled by the Australian Plague Locust Commission (Hunter 2004)). In the United States, massive outbreaks of the Rocky Mountain locust (Melanoplus spretus (Walsh)) were recorded in the 1870s. The largest of the swarms covered a “swath equal to the combined areas of Connecticut, Delaware, Maine, Maryland, Massachusetts, New Hampshire, New Jersey, New York, Pennsylvania, Rhode Island and Vermont” (Riley et al. 1880), and nearly derailed westward expansion. Charles Valentine Riley, now considered one of the founding fathers of entomology in the United States, was appointed by the US government to investigate these outbreaks. His work led him to request further federal assistance, which the government provided in the form of the US Entomological Commission; this agency quickly morphed into the US Department of Agriculture that still operates today. The last known Rocky Mountain locust swarm occurred in the very early 1900s; why it disappeared remains a ­mystery, although some interesting hypotheses have been proposed (Lockwood 2005). The Mormon cricket (Anabrus simplex (Haldeman)) is another orthopteran species renowned for its outbreaks. Populations of Mormon crickets usually occur at low densities throughout most of their range in western North America, but population explosions that exceed more than 1 million individuals, marching in roving bands at densities of more than 100 individuals/m², are not uncommon. In 1848 a Mormon cricket outbreak nearly thwarted the ­settlement of Salt Lake City, Utah, by Mormon pioneers. Although the story is ­controversial, Mormon folklore recounts the miracle of the gulls. Legend claims that legions of seagulls, sent by God, appeared on June 9, 1848. These seagulls saved the settler’s crops by eating all the crickets. South America and Central America also have orthopterans that show outbreak dynamics, the most notable being Schistocerca cancellata (Serville) and Schistocerca piceifrons (Walker), respectively.

Given the devastation and immense suffering inflicted on humans by orthopteran outbreaks, it is pressing to understand the causal factors that contribute to their outbreaks. With the exception of Mormon crickets (see Sword 2005), the orthopterans described above exhibit phase polyphenism – defined by Hardie and Lees (1985, 473) as “occurrence of two or more distinct phenotypes which can be induced in individuals of the same genotype by extrinsic factors.” The African desert locust and African migratory locust are easily two of the best-known ­species to practice phase polyphenism. However, many orthopterans that do not exhibit phase polyphenism can also undergo outbreaks, as has been the case for many grasshopper species in the western United States (Branson et al. 2006).

In this chapter we concentrate primarily on orthopterans, but our aim is to understand factors that contribute to insect herbivore outbreaks more generally. We also discuss other types of insects, particularly lepidopterans, to make our points. Because insect outbreaks cannot happen without an initial increase in population size, we begin by focusing on individuals while considering factors, especially nutritional ones, that contribute to increased performance. We next explore how behavior and performance (e.g., survival, growth, and reproduction) of individual insect herbivores change as population densities increase. Shifting gears, we then discuss how ecological paradigms, particularly the “plant stress hypothesis,” have influenced how we view insect herbivore outbreaks. We conclude the chapter by calling for an integrative approach that translates individual responses into group-level phenomena, couched within the contexts of their communities and ecosystems.

1.2 Which conditions favor the individual, and can lead to insect herbivore outbreaks?

Insect outbreaks are often cyclical and require a confluence of events to occur. Critical is the initial phase of an outbreak – insect herbivores must have access to sufficient food, and that food must be of good quality to ensure survival, rapid growth, and high reproductive output. Historically, plant quality has been defined in terms of its nitrogen content (e.g., McNeil and Southwood 1978, Mattson 1980, Scriber and Slansky 1981), but more recently there has been a shift away from a single currency approach. We now recognize that organisms, including insect herbivores, require a suite of nutrients and perform best when they acquire these nutrients in particular blends (Raubenheimer and Simpson 1999, Behmer 2009, Raubenheimer et al. 2009). Insect herbivores require upwards of 30 dif­ferent nutrients, including protein (amino acids), digestible carbohydrates (e.g., ­simple sugars and starches), fatty acids, sterols, vitamins, minerals, and water (Chapman 1998, Schoonhoven et al. 2005). Plants contain all the nutrients that insect herbivores need, but securing these nutrients in the appropriate amounts and ratios is often challenging because plant nutrient content can be highly variable depending on plant type, age, and growing conditions (Mattson 1980, Scriber and Slansky 1981, Slansky and Rodriguez 1987, Bernays and Chapman 1994).

1.2.1 Factors that influence performance in immature stages

Two particularly important macronutrients for insect herbivores are protein and digestible carbohydrates. Plant proteins provide amino acids (the major source of nitrogen) used to construct insect proteins that serve structural purposes, as enzymes, for transport and storage, and as receptor molecules. In contrast, ­digestible carbohydrates are used primarily for energy, but they can also be converted to fat and stored, and their carbon skeleton can contribute to the production of amino acids. It has long been known that insufficient protein and carbohydrates can limit insect growth and performance.

Only recently, though, have we begun to appreciate the extent to which insect herbivores can regulate the intake of these two nutrients, and that they regulate them independently of one another. The most thoroughly explored insect with respect to protein–carbohydrate regulation is the African migratory locust (the gregarious phase). Laboratory experiments using artificial diets with fixed ­protein–carbohydrate ratios have shown that African migratory locusts regulate their protein–carbohydrate intake under a number of different conditions: (1) when presented with two nutritionally suboptimal but complementary foods (Chambers et al. 1995, Chambers et al. 1997, 1998), (2) as the relative frequency of two nutritionally complementary foods changes (Behmer et al. 2001), (3) as the ­physical space between nutritionally complementary foods increases (Behmer et al. 2003), and (4) in the presence of plant secondary metabolites (Behmer et al. 2002).

A key mechanism that allows Locusta to regulate their protein–­carbohydrate intake involves taste receptors in hundreds of sensilla on and around the ­mouthparts. Each sensillum houses a small set of neurons, some of which are sensitive to amino acids and others to sugars (the other neurons detect water, salt and deterrent chemicals (Chapman 1998)). These neurons operate ­independently, and the sensitivity of the neurons for amino acids and sugars are inversely correlated with the levels of amino acids and sugars in the hemolymph, respectively (Simpson et al. 1990, Simpson et al. 1991, Simpson and Simpson 1992, Simpson and Raubenheimer 1993). Thus, if a locust is starved for protein, the amino-acid neurons are more easily stimulated when high-protein foods are encountered. Likewise, if hemolymph levels of sugar decline, sugar-sensitive ­neurons are stimulated when high-sugar foods are encountered. Self-selected protein and carbohydrate intake points have been identified in a number of insect herbivores, and the functional significance of these self-selected ­protein–­carbohydrate ratio is revealed through no-choice experiments; the self-selected protein–­carbohydrate intake point consistently aligns with the p:c ratio of foods that provide the best performance (Behmer and Joern 2008).

Regulation of other biomolecules, elements, and minerals is less well studied, which represents a serious limitation to understanding how nutrition contributes to outbreaks. Simpson et al. (1990) showed that a suite of 8 amino acids can stimulate amino acid neurons in locusts. One of these amino acids, proline, often elicits increased feeding in caterpillars (Heron 1965, Cook 1977, Bently et al. 1982) and grasshoppers (Cook 1977, Haglund 1980, Mattson and Haack 1987), and this may be functionally significant because free proline concentrations, particularly under drought conditions, are positively associated with concentrations of soluble N in plant tissues (Mattson and Haack 1987). Interestingly, adults of two grasshopper species show a sex-specific response to proline, with females, but not males, preferring proline-rich foods (Behmer and Joern 1994). Perhaps this difference reflects sex-specific nutrient demands; because they invest more in reproduction, females should need more protein than do males. Another amino acid, phenylalanine, is essential and needed in large amount for cuticle ­production by immature insects. In adults it is less important. Using choice-test experiments with fifth-instar and adult Phoetaliotes nebrascensis...

Table of contents

• Cover
• Title page
• Copyright page
• Contributors
• Preface
• PART I: PHYSIOLOGICAL AND LIFE HISTORY PERSPECTIVES
• PART II: POPULATION DYNAMICS AND MULTISPECIES INTERACTIONS
• PART III: POPULATION, COMMUNITY, AND ECOSYSTEM ECOLOGY
• PART IV: GENETICS AND EVOLUTION
• PART V: APPLIED PERSPECTIVES
• Subject Index
• Taxonomic Index
• Colour plates