Molecular Physiology and Evolution of Insect Digestive Systems Walter R Terra Clelia Ferreira Carlos P Silva

Molecular Physiology and Evolution of
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Volume 7
Entomology in Focus
Insects are fundamentally important in the ecology of terrestrial

habitats. What is more, they affect diverse human activities, notably
agriculture, as well as human health and wellbeing. Meanwhile, much of
modern biology has been developed using insects as subjects of study.
To reflect this, our aim with Entomology in Focus is to offer a range
of titles that either capture different aspects of the diverse biology of
insects or their management, or that offer updates and reviews of
particular species or taxonomic groups that are important for
agriculture, the environment or public health.
The series results from an agreement between Springer and the
Entomological Society of Brazil (SEB) and as such may lean towards
tropical entomology. The aim throughout is to provide reference texts
that are simple in their conception and organization but that offer up-
to-date syntheses of the respective areas, offer suggestions of future
directions for research (and for management where relevant) and that
don’t shy away from offering considered opinions.
Editorial Committee
Series Editor Sam Elliot is Associate Professor in Entomology at the
Universidade Federal de Viçosa (Brazil), also coordinates the
Postgraduate Programme in Entomology currently rated maximally by
the relevant authority in Brazil (CAPES) and is Associate Editor at
Ecology and Evolution. He works on diverse aspects of insect-microbe
interactions, with emphases on leafcutter ants, noctuid caterpillars,
triatomine bugs, entomopathogenic fungi and microbial control of
pests.
Adam Hart is Professor of Science Communication at the University
of Gloucestershire (UK). His particular interest is in social insects but
he has written and broadcasted on a broad range of biological subjects.
He presents documentaries for BBC Radio 4, BBC4 and BBC2, as well as
the weekly BBC radio programme Science in Action.
Eugenio Oliveira is Assistant Professor in Entomology at the
Universidade Federal de Viçosa (Brazil), and scholar researcher of the
Brazilian National Council of Scientific and Technologic Development
(CNPq). He has also working as Associate Editor at the journals
Neotropical Entomology and Invertebrate Neuroscience. He works
principally on insect neurophysiology, applying this in particular to
entomological/agricultural questions.
Ken Wilson is Professor of Evolutionary Ecology at Lancaster
University (UK), and is Executive Editor of the Journal of Animal
Ecology. He is particularly interested in host-parasite interactions and
investigates these in invertebrate and vertebrate hosts. Noctuid
caterpillars, especially armyworms, have been one of his main model
systems and he is currently working on their ecology and biocontrol in
Africa.
Walter R. Terra, Clelia Ferreira and Carlos P. Silva
Molecular Physiology and Evolution of

Insect Digestive Systems
Walter R. Terra
Instituto de Química, Universidade de Sã o Paulo, Sã o Paulo, Brazil
Clelia Ferreira
Instituto de Química, Universidade de Sã o Paulo, Sã o Paulo, Brazil
Carlos P. Silva
Departamento de Bioquímica, Universidade Federal de Santa Catarina,
Florianó polis - SC, Brazil
ISSN 2405-853X e-ISSN 2405-8548

Entomology in Focus
ISBN 978-3-031-39232-0 e-ISBN 978-3-031-39233-7
https://doi.org/10.1007/978-3-031-39233-7
© The Editor(s) (if applicable) and The Author(s), under exclusive

license to Springer Nature Switzerland AG 2023
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Dedication: To our families
Preface
The whole field of insect midgut studies was covered in a book entitled
Biology of the Insect Midgut edited by M.J. Lehane and P.F. Billingsley in
1996 (Chapman & Hall, London). Since then, highly efficient techniques
of protein separation were developed and a great amount of molecular
manipulation procedures were introduced or improved, like gene
cloning and production of recombinant proteins, new-generation
sequencing methods, and techniques of suppression of protein
expression. The impact of the use of these methods on midgut studies
was impressive, particularly regarding the molecular mechanisms
underlying digestion and absorption and their evolution. These
advances have been reviewed several times, but never in a
comprehensive book form.
The aim of this book is to provide a balanced blend of introductory
and specialized aspects of the molecular mechanisms underlying insect
midgut buffering, digestion, nutrient absorption, and their changes
along the evolution, ending with a discussion on new technologies of
insect control based on the information gathered in the previous
chapters.
The first part of the book (Chapters 1, 2, 3, and 4) comprises four
major introductory subjects: the omics-based patterns of insect
evolution, to be used to organize the findings in an evolutionary
perspective; overview of the methods and results regarding the spatial
organization of digestion and absorption; description of the types and
chemistry of insect diets; ordinary digestive enzymes that degrade
dietary molecules.
The second part of the book (Chaps. 5, 6, 7, and 8) describes the
organization of midgut cells, the function of their microvillar
membranes and extracellular layers, and, finally, their role in secretory
processes. With this background, the function of membrane
transporters in the absorption of nutrients and maintenance of midgut
pH and water fluxes are detailed.
The third part of the book (Chaps. 8, 9, 10, 11, and 12) deals with
special topics like endocrine regulation of midgut function; adaptations
to overcome the action of digestive enzyme inhibitors; specializations
to deal with plant, bacterial, and fungi cell walls; and, finally, the role of
microorganisms in nutrition.
The last part of the book (Chaps. 13, 14, and 15) reviews the
molecular mechanisms underlying digestion and nutrient absorption in
the major insect orders and postulates how these processes changed
along the evolution. The book ends with an overview of the techniques
of insect control that employs the knowledge gathered along the
midgut studies.
This book was written to be suitable for students and advanced
scientists of entomology, biology, biochemistry, genetics, pest control
specialists, and for those working with degradation of plant cell walls
by insect or midgut microbial enzymes. Work done in the laboratories
of the authors was financed by the Sã o Paulo Research Foundation
(FAPESP, Grant “Temá tico” no. 2017/08103-4), National Council of
Research (CNPq), and National Institute of Science and Technology-
Molecular Entomology (INCT-Entomologia Molecular).
Walter R. Terra
Clelia Ferreira
Carlos P. Silva
São Paulo, Brazil
June 2023
Contents
1 Patterns of Insect Evolution
1.1 Initial Considerations
1.2 Polyneoptera
1.2.1 Dictyoptera
1.2.2 Orthoptera
1.3 Condylognatha
1.3.1 Thysanoptera
1.3.2 Hemiptera
1.4 Holometabola
1.4.1 Coleoptera
1.4.2 Hymenoptera
1.4.3 Diptera
1.4.4 Lepidoptera
References
2 Overview of Insect Midgut Function
2.1 Food Handling and Ingestion
2.2 Gut Morphology
2.3 Stepwise Digestion of Nutrients
2.4 Phases of Digestion and Their Compartmentalization in the
Midgut
2.5 Identification of the Sites of Transport of Water, Ions, and
Nutrients Along the Gut
References
3 Types and Chemistry of Diets
3.2 Detritus
3.2.1 Types of Detritus
3.2.2 Litter Chemical Composition
3.2.3 Litter and Wood Quality
3.2.4 Feces
3.2.5 Carcasses
3.3 Plant Materials
3.3.1 Leaves
3.3.2 Plant Exudates
3.3.3 Pollen
3.3.4 Nectar
3.3.5 Seeds
3.4 Bacteria
3.5 Fungi
3.6 Blood
3.7 Lichen
References
4 Ordinary Digestive Enzymes
4.1 Introduction
4.2 Reliable Enzyme Assays
4.3 Peptidases
4.3.1 Serine Endopeptidases
4.3.2 Collagenases
4.3.3 Carboxypeptidases
4.3.4 Aminopeptidases
4.4 Glycosyl Hydrolases
4.4.1 Amylases and α-Glucosidases
4.4.2 β-Fructosidases
4.4.3 β-N-Acetylhexosaminidases, α-Mannosidases, and α-
Galactosidases
4.4.4 β-Glycosidases
4.4.5 Myrosinase
4.4.6 Trehalases
4.4.7 Lipases and Phospholipases
References
5 Midgut Cells, Microvillar Membranes, and Secretory Mechanisms
5.1 Initial Considerations and Midgut Cell Types
5.2 Enzymes Associated with Midgut Microvilli, Glycocalyx, and
Microvilli-Associated Membranes
5.3 Chemistry of Microvillar and Microvilli-Associated
Membranes
5.4 Mechanisms of Digestive Enzyme Secretion
References
6 Midgut pH Buffering, Nutrient Absorption, Fluid Fluxes, and
Enzyme Recycling
6.1 Overview
6.2 Midgut Conditions That Affect Digestion:pH Buffering,
Redox Media, and Fluid Fluxes
6.3 Ion and Water Transporters
6.4 Nutrient Transporters
6.5 Models of Midgut pH Buffering
6.6 Models of Midgut Fluid Fluxes and Enzyme Recycling
References
7 Midgut Extracellular Layers and Their Function
7.1 Introduction
7.2 Mucus:Chemical Nature and Function
7.3 Peritrophic Membrane:Occurrence, Structure, and
Formation
7.4 Peritrophic Membrane:Evolution and Function
References
8 Endocrine Regulation of Insect Digestion
8.2 The Nervous System and the Regulation of Digestion in
Insects
8.2.1 The Stomatogastric Nervous System of Insects
8.2.2 The Frontal Ganglion
8.2.3 The Hypocerebral Ganglion
8.2.4 The Ventricular Ganglion
8.2.5 The Terminal Abdominal Ganglion
8.2.6 The Midgut Endocrine Cells (Enteroendocrine Cells)
8.2.7 Brain and the Subesophageal Ganglion
8.3 Types of Hormones That Regulate Insect Gut Physiology
8.3.1 AllatoregulatoryPeptides
8.3.2 CCHamides 1 and 2 Peptides
8.3.3 Neuropeptide F and Short Neuropeptide F
8.3.4 Tachykinin-Related Peptides and Insect Kinins
8.3.5 FMRFamide-Related Peptides and Myosuppressins
8.3.6 Insect Kinins
8.3.7 Proctolin
8.3.8 Insect RYamides
8.3.9 Trissin
8.4 Peptidergic Regulation of Insect Digestion
8.4.1 Endocrine Regulation of Mouthparts and Foregut
Functioning
8.4.2 Endocrine Regulation of Midgut Functioning
8.4.3 Endocrine Regulation of Hindgut Functioning
References
9 Recruitment of Lysosomal Cysteine and Aspartic Endopeptidases
as Digestive Enzymes
9.1 Introduction
9.2 Digestive Cathepsins L and B in Coleoptera
9.3 Digestive Cathepsins L and B in Hemiptera
9.4 Digestive Cathepsin D in Diptera Cyclorrhapha, Hemiptera,
and Coleoptera
9.5 Targeting Recruited Lysosomal Enzymes to Midgut Lumen
References
10 Plant, Bacterial, and Fungal Cell Wall-Degrading Enzymes
10.1 Cellulases
10.2 Pectinases
10.3 Hemicellulases
10.4 Laccases
10.5 Exinase
10.6 Chitinases and Lysozymes
References
11 Mechanisms of Avoiding the Action of Plant Inhibitors on
Digestion
11.1 Introduction
11.2 Adaptations to the Ingestion of Plant Inhibitors of
Digestive Endopeptidases
11.2.1 Behavior Adaptation to Avoid Ingestion of PIs
11.2.2 Metabolic Responses to the Ingestion of PIs
11.2.3 Structural Differences Between Sensitive and
Insensitive Digestive Peptidases Toward PIs
11.2.4 Expression of Insensitive or PI-Metabolizing
Endopeptidases
11.2.5 Recruitment of Lysosomal Proteins as Digestive
Cathepsins
11.2.6 Expression of Pseudoendopeptidases
11.3 Mechanisms of Avoiding the Action of Plant α-Amylases
Inhibitors (AIs)
11.3.1 Overview
11.3.2 Adaptation Based on the Occurrence of Multigene
Families of Digestive α-Amylases
11.3.3 Overexpression of AI-Sensitive and AI-Insensitive α-
Amylases
11.3.4 Cleavage of AIs by Digestive Endopeptidases and
Stability of AIs in the Physical-Chemical Conditions
Prevalent in the Intestinal Lumen
11.4 Mechanisms of Avoiding the Action of Plant
Polygalacturonase Inhibitors (PGIPs)
11.4.1 Overview
11.4.2 Adaptation Based on the Expression of Multigene
Families of PGs
11.4.3 Adaptation Based on the Expression of Pseudo-PGs
11.5 Adaptations to the Ingestion of Plant Inhibitors of
Digestive Lipases
References
12 Role of Microorganisms in Digestion and Nutrition
12.1 Introduction
12.2 Bacteria as Food
12.3 Digestion of Recalcitrant Compounds
12.4 Nutrient Provisioning
12.5 Detoxification of Harmful Ingested Compounds
References
13 Molecular View of Digestion and Absorption in the Major Insect
Orders
13.1 Introduction
13.2 Orthoptera
13.2.1 Introduction
13.2.2 Caelifera
13.2.3 Ensifera
13.3 Dictyoptera
13.3.1 Introduction
13.3.2 Blattodea:Cockroaches
13.3.3 Blattodea:Termites
13.3.4 Mantodea
13.4 Phasmatodea
13.5 Phthiraptera
13.6 Thysanoptera
13.7 Hemiptera
13.7.1 Sternorrhyncha
13.7.2 Auchenorrhyncha
13.7.3 Heteroptera
13.8 Megaloptera
13.9 Coleoptera
13.9.1 Introduction
13.9.2 Adephaga
13.9.3 Polyphaga
13.10 Hymenoptera
13.11 Diptera
13.12 Lepidoptera
References
14 General Trends in the Evolution of Digestive Systems
References
15 New Technologies of Insect Control That Act Through the Gut
15.2 Bacterial Insecticidal Proteins Targeting Insect Midgut
Tissue
15.2.1 Membrane Pore-Forming Bt Toxins
15.2.2 Mode of Action of Bt Toxins
15.2.3 Practical Resistance to Bt Toxins
15.3 Digestive Enzyme Inhibitors
15.3.1 Proteinase, α-Amylase, and Polygalacturonase
Inhibitors
15.4 Application of RNAi and CRISPR/Cas Technologies in
Insect Control
15.4.1 Application of RNAi Technology in Insect Pest Control
15.4.2 Application of CRISPR/Caspase Technology in Insect
Pest Control
15.5 Conclusions and Prospects
References
© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
W. R. Terra et al., Molecular Physiology and Evolution of Insect Digestive Systems,
Entomology in Focus 7
https://doi.org/10.1007/978-3-031-39233-7_1
1. Patterns of Insect Evolution

Walter R. Terra1 , Clelia Ferreira1 and Carlos P. Silva2
(1) Instituto de Química, Universidade de Sã o Paulo, Sã o Paulo, Brazil
(2) Departamento de Bioquímica, Universidade Federal de Santa
Catarina, Florianó polis - SC, Brazil
Walter R. Terra (Corresponding author)

Email: [email protected]
Clelia Ferreira
Carlos P. Silva
Abstract
Insects are the most diverse living beings and their ancestors moved
from the sea and colonized the land long before the chordates.
Phylogenetic and fossil data were combined to detail the patterns of
insect evolution. Insects able to flex their wings over the back
(Neoptera) correspond to most of the insects and evolved along the
major lineages: Polyneoptera, Condylognatha, and Holometabola.
Polyneoptera includes Dictyoptera – cockroaches and termites that are
omnivorous or wood feeders and the carnivorous mantids – and
Orthoptera – the omnivorous crickets and grass-feeding grasshoppers.
Condylognatha includes Hemiptera which are the only insects able to
live entirely on plant sap such as aphids, cicadas, and spittlebugs; and
others like bugs adapted to different diets. Holometabola is the most
successful lineage with 86% of the insect species, have complete
metamorphosis (larva, pupa, and adult) and comprises the major insect
orders: Coleoptera (beetles); Hymenoptera (wasps, ants, and bees);
Diptera (mosquitoes and flies); and Lepidoptera (butterflies and
moths). Insects of these orders explore the most diverse food sources
like other insects, stems, leaves and wood, seeds, keratin (like woolen
carpets), pollen, nectar, fungi, and vertebrate blood. The major selective
pressures affecting insect guts identified were: (a) adaptations to deal
with large amounts of dilute fluid food, (b) adaptations to digesting
plant and fungal cells as a result of horizontal transfer of genes from
microorganisms and recruitment of lysosomal proteins as digestive
enzymes, (c) adaptations to avoiding plant inhibitors by gene expansion
and new functionalization, (d) and adaptations to avoiding prolonged
exposure to natural enemies and to living in short-lived media by
reduction of life span permitted by more efficient midguts.

This chapter overviews the patterns of insect evolution, highlighting
the insect taxa and specific insects that are more important for midgut
studies.
Insects are the most diverse living beings and are found in
practically all land surfaces, except in the extreme polar regions and in
the highest mountain peaks (Daly et al. 1998). The success of the
insects is measured by their large number of species amounting to
about half of the known living species and to almost 75% of the
animals. This success is supposed to rely on several of the insect’s
characteristics, such as its exoskeleton, flight capacity, small size, and
ability to use diverse nutritional sources.
The insect exoskeleton made of repetitive segments and
appendages pre-adapted them to walking on land, thus favoring their
exit from the sea and the colonization of terrestrial environments much
earlier than the chordates. Flight permitted the insects to escape from
enemies and find mates, food, and sites to lay eggs. A small size allowed
the insects to live in small places and have short generation time
because less time is necessary to attain adulthood. Finally, the insect’s
capacity to rely on the most varied nutritional sources favors its
adaptation to almost any environment (Daly et al. 1998).
A list of the major insect orders with common names of the most
known insects is shown in Table 1.1.1. This table is expected to make it
easier to follow the description of insect evolution. Non-winged insect
ancestors, together with a few other arthropods, were the first animals
to invade the land, approximately at the same time as plants in the
Early Ordovician (circa 420 Ma) (Grimaldi and Engel 2005; Misof et al.
2014). The most primitive insects were wingless (Infraclass
Apterygotha) and will not be considered here. The first winged insects
(Infraclass Pterygotha) were characterized by wings that cannot be
flexed over the back at rest (Paleoptera) and include Ephemeroptera
(the mayflies) and the predatory Odonata (dragonflies and damselflies).
Neoptera corresponds to most insects, and they have wing flexing that
permits them to enter underneath environments like liter and bark.
Table 1.1 The major insect orders
Infraclass Superorder Order Examples

Paleoptera – Odonata Damselflies, dragonflies
Ephemeroptera Mayflies
Neoptera Polyneoptera Dictyoptera Cockroaches, termites, praying
mantids
Orthoptera Grasshoppers, crickets
Phasmatodea Stick and leaf insects
Condylognatha Hemiptera Bugs, cicadas, aphids
Thysanoptera Thrips
Psocodea Phthiraptera Lice
Psocoptera Booklice
Neuropteroidea Megaloptera Alderflies, dobsonflies
Coleoptera Beetles
Hymenopteroidea Hymenoptera Wasps, bees, ants
Panorpoidea Siphonaptera Fleas
Diptera Mosquitoes, flies
Lepidoptera Moths, butterflies
Infraclass Superorder Order Examples
Trichoptera Caddisflies
Paleoptera, Polyneoptera, and Condylognatha undergo incomplete

metamorphosis, whereas Neuropteroidea and Panorpoidea have
complete metamorphosis
Neoptera evolved along the major lineages Polyneoptera
(Plecoptera, Orthoptera, Phasmatodea, and Dictyoptera);
Condylognatha (Thysanoptera and Hemiptera); and a branch
corresponding to Psocodea (Phthyraptera and Psocoptera) plus
Holometabola (Fig. 1.1). The once proposed clade Paraneoptera,
comprising Condylognatha and Psocodea, is paraphyletic because, as
shown above, Condylognatha is a sister group of
Psocodea+Holometabola. Holometabola includes Hymenoptera and a
large grouping divided into two branches: Neuroptera+Coleoptera and
Panorpoidea. Panorpoidea is divided into two sister clades:
Trichoptera+Lepidoptera and Siphonaptera+Diptera (Fig. 1.1). The
expansion of Hymenoptera, Diptera, and Lepidoptera occurred in
parallel with the radiation of angiosperms in Early cretaceous (circa
100 Ma) (Misof et al. 2014).
Fig. 1.1 Simplified phylogenetic tree of the relationships of the major insect orders.
Number in nodes mean: 1, Pterygotha; 2, Paleoptera; 3, Neoptera; 4, Polyneoptera; 5,
Condylognatha; 6, Psocodea; 7, Holometabola; 8, Panorpoidea. Geological periods:
Devonian, Carboniferous, Permian, Triassic, Jurassic, Cretaceous. (Details in text)
Holometabola comprises 86%, Polyneoptera (mainly Orthoptera
and Dyctioptera) 3.2%, and Condylognatha (mainly Hemiptera) 7.1% of
the insect species. The evolutionary success of Holometabola is
supposed to result from the fact that their young forms (larva) are
adapted to ecological niches different from those of adults, thus
avoiding their competition for the same food, as occurs with insects
without complete metamorphosis (Polyneoptera, Condylognatha, and
Psocodea). After this overview of insect evolution, the major insect
orders will be reviewed, calling attention to some remarkable species
that are subject of studies of their digestive systems and, finally, their
internal phylogenetics will be discussed.
1.2 Polyneoptera
1.2.1 Dictyoptera
Dictyoptera comprises Blattodea (cockroaches and termites) and
Mantodea (mantis). Cockroaches are believed to be ancient insects
arising in the Carboniferous. However, though modern families evolved
since the Cretaceous and are usually omnivorous, some species only
feed on dead wood (wood roaches) (Grimaldi and Engel 2005). Mantids
are usually carnivorous with some species feeding on pollen as a
complement (Beckman and Hurd 2003). Blattodea includes Blattidae,
the most ancient group of modern cockroaches, exemplified by
Periplaneta americana (American cockroach) and Blata orientalis
(Oriental cockroach), and two other major branches: the branch
Cryptocercidae-Termitidae, where one finds the termites that are no
longer considered to be a separate order (Isoptera) (Inward et al.
2007), and the branch Ectobiidae (early Blatellidae)-Blaberidae. An
example of Ectobiidae is Blatella germanica and of Blaberidae are the
wood roaches Panesthia cribata and Nauphoeta cineri (Grimaldi and
Engel 2005).
Lo et al. (2007) agree with Inward et al. (2007) that the order
Isoptera should be dismissed. However, they think that the name
Termitidae should not be employed to refer to all termites, because
Termitidae is still in use to describe the more derived termites. We
accepted this argument and will refer to all termites as the “taxon of
termites” and will maintain the traditional division of families and
subfamilies of the old order Isoptera.
1.2.2 Orthoptera
Orthoptera are the dominant group of chewing hemimetabolous
insects. The ancestors of Orthoptera gave rise to the crickets (suborder
Ensifera, exemplified by Gryllodes sigillatus), which are omnivorous or
predatory, and the grasshoppers (suborder Caelifera like Abracris
flavolineata), which feed mainly on grasses. Locusts are grasshoppers
that periodically form large populations, attacking one and then
swarming to other places. Locusta migratoria, the migratory locust, is
the most widespread locust species being found mainly in all of Africa,
Australia, and New Zealand. Schistocerca gregaria, the desert locust, is
found primarily in Africa, Arabia, and West Asia. The phylogeny of
Orthoptera is discussed by Zhang et al. (2013).
1.3 Condylognatha
1.3.1 Thysanoptera
Thysanoptera (thrips) is sister of the order Hemiptera and together
forms the taxon Condylognatha. Thysanoptera have piercing-sucking
mouthparts like Hemiptera, but less specialized for sucking fluids. The
mouthparts are usually too short to tap into the vascular system of the
plants. Feeding thrips perforate the surface of the plant tissues (their
most common food) and insert their mouthparts in them. Then, in back
and forth movements, fluid, particles of plants, or prey (in predatory
thrips) are ingested (Grimaldi and Engel 2005).
1.3.2 Hemiptera
Hemiptera corresponds to about 7.1% of the insect species and are
surpassed in number of species only by the holometabolous order of
Coleoptera, Hymenoptera, Lepidoptera, and Diptera. The internal
phylogenetic relationships of Hemiptera are summarized in Fig. 1.2 and
discussed in detail by Johnson et al. (2018). Only Hemiptera developed
a sap-sucking habit, though insects of many other orders have suitable
piercing-sucking mouthparts. Thus, it is likely that the sap-sucking
habit depends on modifications in the midguts that enable hemipterans
to deal rapidly with large amounts of dilute fluid food.
Fig. 1.2 Simplified phylogenetic tree of the relationships of the major Hemiptera
taxa. Numbers in nodes: 1, Sternorrhyncha; 2, Auchenorrhyncha; 3, Heteroptera; 4,
Cimicomorpha; 5, Pentatomomorpha. (Details in text)
Hemiptera ancestors on evolution gave origin to Sternorrhyncha
(aphids and white flies), exemplified by Acyrthosiphon pisum, which
together with Auchenorrhyncha (cicadas, spittlebugs, leafhoppers, and
planthoppers), like Homalodisca vitripennis and Nilapavarta lugens,
usually feed on plant sap, either from the phloem or xylem.
Phloem fluid sap is transported downward through the outer layers
of the plant stems. It is usually rich in sugars, with significant amounts
of free amino acids, potassium, and some organic acids. Some phloem
fluids are rich in proteins, functioning in wound signaling and plugging
the sieve elements to avoid nutrient loss. Other proteins are involved in
defense against herbivorous and phloem feeders, exemplified by
protease inhibitors and lectins (Kehr 2006; Zhang et al. 2012). Xylem
fluid is transported upward through the inner layers of the plant stems,
containing large amounts of potassium and trace amounts of amino
acids and sugars (Lopez-Millan et al. 2000). There are also small
quantities of proteins active in repair and defense that are taken up or
produced by the roots (Buhtz et al. 2004).
Sternorrhyncha sucks phloem sap. A shift to xylem feeding, which is
more internal than phloem, coincided with the origin of Cicadomorpha
among Auchenorrhyncha (Johnson et al. (2018). Both Sternorrhyncha
and Auchenorrhyncha excrete honeydew (excess sugar ingested by the
insects), but Sternorrhyncha excrete more, often several times the body
weight of the insect per day (Grimaldi and Engel 2005). The honeydew
is collected by ants.
Heteroptera are adapted to different diets and have two major
infraorders Cimicomorpha and Pentatomomorpha. Among the
Cimicomorpha, the largest family are the Miridae (plant bugs),
exemplified by Lygus sp. and the bed bug Cimex lectularis. Another large
family of Cimicomorpha is Reduviidae, thought to be the basal group of
the infraorder and its most studied representative is Rhodnius prolixus.
The largest families of Pentatomomorpha are the Pentatomidae that
have scent glands (e.g., Nezara viridula) and virtually all feed on plant
sap or fruit, rather than on vegetative tissues, whereas the Lygaeoidea
(e.g., Oncopeltus fasciatus, the common milkweed bug, and
Halyomorpha halys, the brown marmorated stink bug) and
Pyrrhochoridae (e.g., Dysdercus peruvianus) are seed-sucker bugs
(Weirauch et al. 2019).
1.4 Holometabola
1.4.1 Coleoptera
Coleoptera is the most successful order of Holometabola, corresponding
to about 35% of the insect species. This success probably is a
consequence of Coleoptera being the first land insects with complete
metamorphosis to massively occupy hidden niches on the ground
(Grimaldi and Engel 2005). Furthermore, there was an adaptive
radiation of specialized herbivorous beetles (Phytophaga), following
the horizontal transfer of microbial genes encoding plant cell wall–
digesting enzymes (see Chap. 10). Those enzymes made possible beetle
leaf and seed mining and stem and wood boring.
The internal phylogenetic relationships of Coleoptera are
summarized in Fig. 1.3 and discussed in detail by Zhang et al. (2018)
and McKenna et al. (2019). The beetle ancestor gave rise to the major
suborders Adephaga and Polyphaga with the infraorders Elateriformia,
Staphyliniformia, Scarabaeiformia, Bostrichiformia, and Cucujiformia
(Zhang et al. 2018; McKenna et al. 2019). Adephaga are the largely
predaceous ground and water beetles comprising approximately 10%
of all beetles, most of which are from the family Carabidae (e.g.,
Pheropsophus aequinoctialis).
Fig. 1.3 Simplified phylogenetic tree of relationships of the major Coleoptera taxa.
Numbers in nodes: 1, Adephaga; 2, Polyphaga; 3, Elateriformia; 4, Staphyliniformia; 5,
Scarabaeiformia; 6, Bostrichiformia; 7, Cucujiformia; *, Phytophaga. (Details in text)
Among Polyphaga, Elateriformia is sister of a branch comprising

two taxons: Staphyliniformia+Scarabaeiformia and
Bostrichiformia+Cucujiformia. The major superfamilies of Elateriformia
are Buprestoidea, with a single family of metallic wood-boring beetles
(Buprestidae, jewel beetles), and Elateroidea, exemplified by the
luminescent beetles of the family Elateridae (click beetles as
Pyrophorus divergens and Pyrearinus termitilluminans) and Lampyridae
(fireflies exemplified by Aspisoma lineatum) that feed using extraoral
digestion. For this, they regurgitate onto their preys and suck the partly
digested material (Grimaldi and Engel 2005).
Scarabaeidae in the superfamily Scarabaeoidea is the largest family
of the group, including the well-known dung-rolling beetles (dung
beetles) that occur throughout the world, mainly in tropical grasslands.
Females periodically lay eggs on the dung balls, which serve as food for
the larvae (Grimaldi and Engel 2005). The most studied scarabs are
Oryctes nasicornis, Costelytra zealandica, and Pachnoda ephippiata.
Bostrichiformia, a sister taxon of Cucujiformia, includes the family
Dermestidae, the carpet beetles that feed on keratin (like woolen
carpets) and the very dry proteinaceous remains of carcasses,
exemplified by Dermestes maculatus. Among Cucujiformia,
Coccineloidea is sister of the remaining superfamilies of the infraorder,
which grouped into Cucujoidea (which now includes Phytophaga) and
Cleroidea+Tenebrionoidea. Old lineage Cucujoidea is paraphyletic, as
Phytophaga was recovered by McKenna et al. (2019) within Cucujoidea.
Phytophaga comprises the superfamilies Curculionoidea (weevils, e.g.,
Sphenophorus levis), from which the main family is Curculionidae and
Chrysomeloidea, with major families Chrysomelidae and Cerambycidae.
Chrysomelidae includes a subfamily Bruchinae that borrow seeds
which contain toxins. Examples are the chewing seed beetles
Callosobruchus maculatus and Zabrotes subfasciatus. Cerambycidae
(long-horned beetles, e.g., Migdolus fryanus) feed as adults on leaves
bark and sometimes pollen, whereas the larvae mine the phloem of
trees and bore wood.
The largest family of Tenebrionoidea is Tenebrionidae. They are
generally scavengers on dried plant remains, but also feed on lichens,
fungi, and decaying wood. Important pests of stored grain and insect
models are the flour beetles Tribolium castaneum and Tenebrio molitor
(Grimaldi and Engel 2005).
1.4.2 Hymenoptera
Hymenoptera is traditionally divided into Symphyta (sawflies and
horntails or wood wasps) and Apocrita, which comprises Parasitica,
parasites of other insects, and Aculeata, in which the piercing
ovipositor of Parasitica evolved into a stinging organ (Grimaldi and
Engel 2005). Extensive phylogenetic studies detailed the evolution and
the internal phylogenetic relationships of Hymenoptera (Peters et al.
2017). It is now accepted that Symphyta is paraphyletic and some old
clades were reorganized.
The basal lineage of Hymenoptera (Eusymphita) is formed by
sawflies that are external leaf feeders of the superfamilies
Pamphilioidea and Tenthredinoidea (which resemble caterpillars, e.g.,
Themos malaisei) or are wood wasps that bore wood as larvae. Among
the endophytic sawflies lineages, Orussoidea (parasitoid wood wasps)
are the closest relatives of Apocrita (waisted wasps). The rapid
diversification of Apocrita is thought to be helped by the evolution of
the wasp waist, a constriction between abdominal segments that favor
movements of the abdomen, including the ovipositor. Apocrita evolved
along two major lineages: Parasitoida (parasitoid wasps, e.g., Bracon
hebetor), characterized by endoparasitism and miniaturization, and
Aculeata (stinging wasps). Aculeata evolved from lineages close to
Parasitoida, whose females used their ovipositor to sting and
immobilize the host larvae. Wasp females then lay eggs on the host and
their larvae develop inside them. Parasitoida includes Ichneumonoidea,
Chalcidoidea, and Cynipoidea (respectively ichneumon, chalcid, and gall
wasps).
Aculeata gave origin to Vespoidea and Formicidae-Apoidea.
Vespoidea comprises the potter, honey, and social wasps. Potter or
mason wasps are so named because of their mud nests; honey wasps
because they produce honey, and social wasps, which are also known as
paper wasps, because they build and live in communal nests of a paper-
like material made by mixing wood fibers with saliva. Formicidae are
the ants and Apoidea comprises digger wasps (Crabonidae) and the
bees (Anthophila). Ants are among the most ubiquitous insects
amounting in number of individuals to about 1% of all insects. All ants
are social insects and may be herbivorous, scavengers, or predators,
and some collect seeds or pieces of leaves and flowers on which they
cultivate the fungus they eat (leaf-cutting ants of the tribe Attine). Bees
(e.g., Apis mellifera and Scaptotrigona bipunctata) originate in evolution
within the apoid wasp family Crabonidae with a change from a
predatory to a herbivorous (pollen gathering) lifestyle associated with
the diversification of angiosperms, which was followed by a great
expansion of bees. A table detailing the evolution of food habits of
Hymenoptera is found in Daly et al. (1998).
1.4.3 Diptera
Diptera account for about 15% of insect species and are the most
ecologically variable group of insects, repeatedly changing between
habits and habitats along the evolution. Most Diptera are saprophytes
(consumers of vegetal or animal remains) and their larvae are
predominantly found in wet media. There were several independent
origins of predation, phytophagy (plant feeding), mycophagy (fungus
feeding), hematophagy (vertebrate blood feeding), myiasis (internal
feeding in vertebrates), besides the basal habit of saprophagy and dung
feeding (coprophagy) (Wigmann and Yeats 2017). A list of habitats and
feeding food habits of Diptera is found in Daly et al. (1998). As a
consequence of the remarkable diversification of Diptera, the study of
their internal phylogenetic relationship is difficult and is still underway
(Yeats et al. 2007; Wigmann and Yeats 2017).
Traditionally Diptera is divided into two suborders: Nematocera
and Brachycera. Nematocera include the most structurally primitive
Diptera and according to modern studies employing a phylogenetic
approach it is paraphyletic, whereas Brachycera is monophyletic. There
is a trend now to recognize four infraorders corresponding to the old
Nematocera clade: Tipulomorpha, Culicomorpha, Psychomorpha, and
Bibionomorpha (Wigmann and Yeats 2017).
Culicomorpha include Chironomidae (midges, exemplified by
Chironomus thummi), Culicidae (mosquitoes as Aedes aegypti and
Anopheles gambia), and Simuliidae (blackflies, usually of the genus
Simulium). Culicomorpha larvae are plankton feeders living in standing
water (Culicidae) or feeders of organic matter at the bottom of bodies
of water (Chironomidae). The adult forms do not feed (Chironomidae),
and others feed on nectar (Simuliidae and Culicidae males) or on
vertebrate blood (Simuliidae and Culicidae females) (Daly et al. 1998).
Psycomorpha includes the psychodidae blood-feeders and disease
vector Phlebotomus. Bibionomorpha comprises 17 families, exemplified
by Mycetophilidae (fungus gnats) and Sciaridae (black fungus gnats,
e.g., Rhynchosciara americana), which usually are litter decomposers in
forests.
Brachicera is divided into a branch with three infraorders, one of
which is Tabanomorpha, plus Muscomorpha, which includes two
superfamilies and Eremoneura. Tabanomorpha includes Tabanidae
(horse flies), which cut the skin of the host with their blade-shaped
mandibles and then lap up the flowing blood. Eremoneura comprises
two branches: one containing a single superorder (Empidoidea) and
Cyclorrhapha, a large grouping with seven superorders, from which the
more important are Muscoidea, Oestroidea, and Acalyptrata. Well-
known Muscoidea insects are the housefly (Musca domestica,
Muscidae), the tsetse fly (Glossina palpalis, Glossinidae), and the stable
fly (Stomoxys calcitrans, Muscidae).
Among the Oestroidea, there are the grey flesh fly Sarcophaga
bullata and the blow fly Calliphora erytrocephala, which are important
in the field of forensic entomology, because of their value in post-
mortem interval estimation. Other blow flies like Lucilia cuprina lay
eggs in wounds of living animals, causing myiasis, and even in humans
and may result in huge livestock losses. The horse bot fly Gasterophilus
intestinalis lives inside horse stomachs as larvae.
Finally, Acalyptrata includes the leaf-miners Agromyzidae, the true
fruit flies (Tephritidae, exemplified by Ceratitis capitata and
Anastrepha), and the laboratory fruit flies of the geneticists, Drosophila
melanogaster (Drosophilidae). Tephritidae are named true fruit flies
because they usually attack fruits of living plants, whereas
Drosophilidae actually are fungus feeders that acquired the name fruit
fly because they feed on decaying fruit.
Most Brachycera larvae feed on decaying plants (Drosophilidae) or
animals (Muscidae, Calliphoridae, Sarcophagidae), although they may
be also predatory (Asilidae, robber flies), herbivorous or scavengers
(Tabanidae), leaf and stem miners (Agromyzidae, leaf miner flies),
parasites of insects (Tachinidae) or of mammals (Gasterophilidae), and
inhabitants of fruits (Tephritidae). Brachycera adults may be predatory
(Asilidae), pollen feeders (Syrphidae, the hover flies) and blood feeders
(e.g., Tabanidae females, the horn fly Haematobia irritans, the stable fly
Stomoxys calcitrans, and the tsetse fly Glossina palpalis), but most feed
on nectar or liquids associated with decaying material (Daly et al.
1998).
1.4.4 Lepidoptera
Lepidoptera (butterflies and moths) amounts to about 13% of the insect
species and originated in the Late Carboniferous (about 300 Ma) with
mandibulate adults and larvae feeding externally on nonvascular land
plants (Bryophites: hornworts, mosses, liverworts). In the Middle
Triassic (about 241 Ma), a long coiled tube-like proboscis evolved,
which allowed lepidopterans to acquire nectar from flowering plants
(Kawahara et al. 2019). Hearing organs appeared independently in
several lineages of moths, before the origin of bats, pre-adapting them
to detect the bat sonar, which permitted them to avoid bat predation
(Kawahara et al. 2019).
Extant species of Lepidoptera include basal lineages and the clade
Ditrysia, containing the great majority of species. Ditrysia comprises
several superfamilies like Tineoidea (e.g., Tineola bisselliela, the
common clothes moth), Tortricoidea (e.g., the leaf rollers of the family
Tortricidae), and Papilionoidea (butterflies) that is the sister group of
all remaining moths superfamilies, exemplified by Pyraloidea (snout
moths, which includes the Pyralidae Ephestia kueniella and the
Crambidae Diathraea saccharalis); Noctuoidea (miller moths as
Spodoptera frugiperda); Bombycoidea comprising the families
Bombycidae (e.g., the familiar silkworm, Bombyx mori), Sphingidae
(e.g., the cassava hornworm, Erinnyis levis and the tobacco hornworm,
Manduca sexta); and Saturniidae (e.g., the giant silkworm moth,
Hyalophora cecropia). Other details of the internal phylogenetic
relationships of Lepidoptera are discussed by Kawahara et al. (2019).
Adults usually feed on nectar, honeydew, or fermenting sap with their
proboscis, whereas larvae as a rule are external feeders of higher
plants, which nearly all are attacked by at least one species of
Lepidoptera.
According to the patterns of insect evolution discussed above, the
major selective pressures affecting insect guts identified were: (a)
adaptations to deal with large amounts of dilute fluid food (see Chap.
13 under Hemiptera); (b) adaptations to digesting plant and fungal
cells as a result of horizontal transfer of genes from microorganisms
and recruitment of lysosomal proteins as digestive enzymes (see Chaps.
9 and 10); (c) adaptations to avoiding plant inhibitors by gene
expansion and new functionalization (see Chap. 11); and (d)
adaptations to avoiding prolonged exposure to natural enemies and to
living in short-lived media by reduction of life span permitted by more
efficient midguts (see Chap. 14).
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© The Author(s), under exclusive license to Springer Nature Switzerland AG 2023
W. R. Terra et al., Molecular Physiology and Evolution of Insect Digestive Systems, Entomology in
Focus 7
https://doi.org/10.1007/978-3-031-39233-7_2
2. Overview of Insect Midgut Function

Walter R. Terra1 , Clelia Ferreira1 and Carlos P. Silva2
(1) Instituto de Química, Universidade de Sã o Paulo, Sã o Paulo, Brazil
(2) Departamento de Bioquímica, Universidade Federal de Santa Catarina,
Florianó polis - SC, Brazil
Walter R. Terra (Corresponding author)

Clelia Ferreira
Carlos P. Silva
Abstract
Food may be acquired by biting with chewing parts, sucking by pierce-sucking
mouthparts, or by ingesting a pre-digested or pre-dispersed meal. Digestion is a
stepwise process by which the molecules of food are hydrolyzed into components
able to be absorbed. The first step of digestion is the initial digestion, when food
polymers result in oligomers, followed by the second step, intermediary digestion,
corresponding to the conversion of oligomers into dimers and, finally, the third
step, final digestion, in which the dimers are cleaved into monomers that are
absorbed. The gut morphology varies among insect taxa from the basal plan
formed by a capacious crop followed by a midgut with anteriorly placed ceca,
ending in a hindgut. The midgut has inside an anatomical chitin-protein film, the
peritrophic membrane (PM), that separates two luminal compartments:
endoperitrophic (inside PM) and ectoperitrophic (outside PM) spaces. In
polyneopterans and lower holometabolans, the enzymes of initial and
intermediary digestion move freely inside the midgut, whereas in higher
holometabolans, only the enzymes of initial digestion traverse PM into the
endoperitrophic space. The enzymes of intermediary digestion are retained in the
ectoperitrophic space because they are larger than the PM pores (7–9 nm dia).
There are midgut countercurrent fluxes caused by the secretion of fluid in a
posterior region and its absorption in an anterior region. These countercurrent
fluxes decrease the loss of enzymes by excretion as part of the enhancement of
digestive efficiency caused by the compartmentalization of digestion. The sites of
water and nutrient absorption are identified with the use of a non-absorbable dye
and nutrients. The concentration of dye indicates water removal, its dilution
indicates water secretion, whereas a change in the ratio of nutrient and dye
indicates nutrient absorption.
2.1 Food Handling and Ingestion

Digestion is the process by which the molecules in the food once ingested are
hydrolyzed into smaller units that can be absorbed by the gut cells. The gut is
responsible for all steps of food processing after ingestion: digestion, absorption,
formation of feces, and their delivery.
Food must be prepared before ingestion, and this process depends on the kind
of food, insect mouthparts, and insect habits. The most usual form of acquiring
solid food is by biting with chewing mouthparts lubricated with saliva. In this
case, the saliva usually is devoid of digestive enzymes. Occasionally, the saliva
contains amylase and α-glucosidase (Walker 2003), and in rarer cases, as
observed in cockroaches, it has also laminarinase and cellulase (Genta et al.
2003). It should be noticed, however, that salivary enzymes have only a subsidiary
role in digestion (see Table 2.1 as an example), as most digestion is actually
carried out by midgut enzymes. Another way of ingesting solid food is after
extraoral digestion, which will be detailed below.
Table 2.1 Representative digestive enzymes in salivary glands and different gut sites of Abracris
flavolineata (Orthoptera) adults
Foregut Midgut
Enzyme Salivary gland Crop Caeca Ventriculus Hindgut
Amylase 5.3 40.5 39.2 12.9 7.4
Trypsin 0.03 30.4 40.3 21.4 7.9
Maltase 0.09 54.0 26.0 10.8 9.2
Aminopeptidase 0.11 23.0 49.0 20.9 7.1
Trehalase 11.1 20.5 17.0 32.0 20.7
Data according to Ferreira et al. (1990). Figures are % activity in relation to total
gut
Liquid food usually is nectar, blood, or plant sap. Nectar is taken by lapping up
(bees) or sucking (adult lepidopterans) mouthparts. Blood is acquired with
piercing-sucking mouthparts in a fast and painless process to avoid host reaction
thanks to the presence in the saliva of analgesics, vasodilators, and anticoagulants,
but without digestive enzymes (Arca and Ribeiro 2018). Plant sap is taken by
hemipterans with the aid of pierce-sucking mouthparts. Their mouthparts consist
in a stylet that are used to penetrate the diet and have two channels: one for
injecting salivary fluids and another for the inflow of the diet. Sap-sucking
hemipterans have a kind of saliva that form a sheath surrounding the stylets and
another containing enzymes to facilitate access to the plant conducting vessels
(Walker 2003). This is usually known as the stylet-ensheath mechanism (see
other details in Chap. 13). As this mechanism is one kind of extraoral digestion,
this will be detailed below.
Extraoral (or preoral) digestion is the enzymatic treatment of food before
ingestion. This strategy is used mostly by predaceous insects, which usually
regurgitate midgut contents over the prey (reflux extraoral digestion) and after a
while re-ingest the partially digested material from the prey (Cohen 1995; Canton
and Bonning 2020). Enzymes involved in the reflux extraoral digestion include all
enzymes found in the midgut luminal contents, which are those responsible for
initial and intermediary digestion. This was shown, for example, by stimulating
predaceous larvae of Pyrearinus termitilluminans with balls of absorbent paper.
After several attempts, the larvae attack the paper balls and regurgitate over
them. The digestive enzymes recovered from the balls were qualitatively and
quantitatively the same as those occurring in midgut contents. Enzymes carrying
final digestion are restricted to midgut cells (Colepicolo-Neto et al. 1986).
Another type of preoral digestion (non-reflux extraoral digestion) is actually a
dispersion of the tissues of the prey (either animal or vegetal) by digesting the
intercellular cement with digestive fluids produced and secreted by specialized
organs, usually the salivary glands (Cohen 1995; Canton and Bonning 2020). This
kind of preoral digestion is found mainly among hemipterans. In the plant sap–
feeding hemipterans, the enzymes usually employed to assist in plant penetration
by breaking the extracellular matrices are mainly pectinases, glucanases, and
cellulases (Sharma et al. 2014; Tan et al. 2016). Some metalloprotease are able to
degrade the sieve tube proteins occur in aphid saliva, improving nutrition by
complementing the usually poor phloem sap (Canton and Bonning 2020).
Phytophagous Heteroptera are not sap feeders and they access their plant diet in
a lacerate and flush mechanism, which consists of the repeated insertion and
withdrawal of the stylet. The pierced plant tissue is then flushed with saliva that
disperses it employing the same kind of enzymes as the sap feeders. Predaceous
hemipterans disperse the tissues of their preys by a lacerate and flush mechanism
with enzymes like salivary collagenase that degrades the fibers of collagen, one of
the constituents of the extracellular matrix in animals. The once-ingested tissue
fragments of preys (observed in midgut contents) are further digested in the
midgut (Fialho et al. 2012).
The evolutionary advantage of the extraoral digestion in comparison with the
acquisition of food by biting the prey and ingesting it in piece meals is that it
avoids the ingestion of indigestible tissues as the arthropod exoskeletons and
perhaps also provides a defense against pathogens and noxious chemicals in the
diet. In the case of sap and phytophagous hemipterans, saliva may also contain
proteins affecting plant defenses, like a calcium-binding protein that suppresses
phloem sieve occlusion to prevent sap loss following injury (Will et al. 2007,
2009).
Finally, there is another form of extraoral digestion found among wood-
feeding Siricidae (Hymenoptera). The larvae of these insects have modified mouth
parts that press fungus-attacked xylem and squeeze out the nutritious material
that is subsequently ingested and further digested (Thompson et al. 2014).
2.2 Gut Morphology

A generalized diagram of the insect gut is shown in Fig. 2.1. Foregut and hindgut
cells are covered with a cuticle, which is non-permeable to most molecules in the
foregut, but which is permeable to water, ions, and some organic compounds in
the hindgut. Midgut cells lack a cuticle but are separated from the midgut contents
by a film-like anatomical structure named peritrophic membrane (PM). PM
divides the midgut contents into endoperitrophic (inside PM) and ectoperitrophic
(outside PM) spaces. The foregut begins with the mouth, followed by the cibarium
(see below), pharynx, and esophagus, which is linked to the crop (a storage organ)
and an organ (proventriculus), which is a triturating device in some insects,
whereas in most insects it is only a valve controlling the entrance of food into the
midgut. The midgut comprises a tube (ventriculus) from which may branch blind
sacs (gastric or midgut ceca). Anteriorly placed midgut ceca are involved in
digestion and water and nutrient absorption, whereas midgut ceca placed
elsewhere are implicated in other functions (details below). In some insects,
usually blood-feeders, the anterior midgut is dilated and stores food. In these
cases, the anterior midgut is frequently named stomach. The Malpighian tubules
(an excretory organ) branch from the gut at the region of the sphincter (pylorus)
that separates the midgut from the hindgut, and in a few insects they are joined to
form a ureter (Fig. 2.2b). The hindgut comprises the ileum, colon, and rectum and
ends at the anus, but may be modified in a fermentative chamber harboring
microorganisms that may assist cellulose degradation (see Chaps. 10 and 13). The
gut epithelium is surrounded by longitudinal and circular muscles that propel the
food bolus along the gut by peristalsis that are wave-like contractions of the
circular muscles. The gut is oxygenated by the tracheal system and is more
innervated at the fore- and hindgut than in the midgut. Visceral muscles connect
the gut to the body wall and act as dilators of the gut. In the foregut, those muscles
form a pump mainly developed in fluid feeders (cibarial pump). In chewing
insects, the dilator muscles form the pharyngeal pump that enables the insects to
drink water and pump air during the molts.
Fig. 2.1 Generalized diagram of the insect gut showing the sites of important digestive events
and water fluxes (dotted arrows) and the circulation of digestive enzymes (solid arrows)
Fig. 2.2 Major insect gut types. Ad adult, AV anterior ventriculus (midgut), C crop, Co colon, E
esophagus, F fermentation chamber, FC filter chamber, G midgut (gastric) ceca, I ileum, La larva, M
Malpighian tubules, MgP midgut protuberances, MgT midgut tubules, Mx Mixed segment, P
proventriculus, Pa paunch, P1-5 hindgut regions in termites, PV posterior ventriculus, R rectum, U
ureter, V ventriculus. Not drawn to scale. (Based partly in Terra WR (1988). Physiology and
biochemistry of insect digestion: An evolutionary perspective. Braz J Med Biol Res 21: 675–734)
Gut morphology varies widely among insects from different orders and
between the larvae and adults in most holometabolan insects. As we are
interested in insect digestion and absorption, emphasis will be given only to the
insect stages that are notorious feeders. From this point of view, young and adult
forms of Polyneoptera and Condylognatha perform similarly and have similar gut
morphologies, whereas among the holometabolan, except for some blood- and
pollen-feeders only the larval forms will be considered (Fig. 2.2). Those interested
in a more detailed presentation of gut morphologies should consult Snodgrass
(1935), Chapman (1985), and Simpson and Douglas (2013).
Polyneoptera insects have a capacious crop and anteriorly placed midgut ceca,
which are absent from Dictyoptera Termitidae and Mantodea (Fig. 2.2a–f). The
enlargement of hindgut structures in Dictyoptera Blattodea and Termitidae that
are involved in dealing with wood and other cellulosic materials is noticeable (see
Chaps. 10 and 13). Phasmatodea have a kind of posteriorly placed midgut ceca
resembling Malpighian tubules known as midgut tubules supposed to be active in
midgut alkalization (Monteiro et al. 2014) (Fig. 2.2a–f).
Hemipterans lack PM, crops, and anteriorly placed midgut ceca (Fig. 2.2g–i).
Some Pentatomomorpha have posteriorly placed midgut ceca in contact with the
anterior parts of the ventriculus (Fig. 2.2i) and are assumed to have a function
similar to the filter chamber of Auchenorrhyncha and Sternorrhyncha insects
(Goodchild 1963). The filter chamber is a structure formed by the apposition of
the posterior midgut and the proximal ends of the Malpighian tubules to the
anterior midgut, thus facilitating the passage of water directly from the anterior
midgut to the Malpighian tubules, resulting in the concentration of dilute food (Le
Cahérec et al. 1997).
Holometabola guts are variable. Megaloptera and primitive Coleoptera have
crops but lack anteriorly placed midgut ceca, with exceptions like Coleoptera
Dermestidae (Caldeira et al. 2007). Except for some adult insects (Hymenoptera
Apidae, Diptera Culicidae, and Lepidoptera), holometabolous insects do not have
crops. Anteriorly placed midgut ceca are only found in mosquitoes and midges.
Coleoptera Scarabaeidae have midgut ceca organized in rings along the midgut
(Fig. 2.2l) and Hymenoptera Tenthredinoidea have a ring of ceca disposed in U
format in the ventral side of the anterior midgut (Fig. 2.2n). In both cases, the ceca
are thought to be involved in the alkalization of midgut contents (see details in
Chap. 6).
2.3 Stepwise Digestion of Nutrients

Most food molecules are polymers and must be reduced to monomers to be
absorbed. Digestion of polymers (proteins and starch) occurs in three phases:
initial, intermediate, and final (Fig. 2.3). Initial digestion is carried out by enzymes
that cleave the internal bonds of the polymers (e.g., endopeptidases in the case of
proteins and amylase for starch). During intermediate digestion, oligomers
(oligopeptides and oligosaccharides) are split into dimers by, respectively,
carboxypeptidases and amylases. In sequence, during the final digestion, the
dimers (dipeptides and maltase) are hydrolyzed by dipeptidases and maltases.
Aminopeptidases are active on small oligopeptides and also on tri- and
dipeptides. Thus, aminopeptidases are active in the final digestion of proteins in
combination or in replacement of dipeptidases. Likewise, α-glucosidases act on
small oligosaccharides and disaccharides and, hence, they are responsible for the
final digestion of starch. When the α-glucosidases hydrolyze only maltose they are
named maltase.
Fig. 2.3 Stepwise digestion of nutrients. Arrows point to the chemical bonds hydrolyzed by the
identified enzymes. (a) Protein digestion; R, different amino acid moieties; (b) starch digestion;
(c) β-linked glucoside; (d) lipid digestion; PL phospholipase, R fatty acyl moieties. (Reprinted
with permission from Terra WR, Ferreira C, 2012. Biochemistry and molecular biology of
digestion., in: Gilbert, L.I. (Ed.), Insect Molecular Biology and Biochemistry. Academic
Press/Elsevier, London, pp. 365–418)
The endopeptidases usually involved in insect digestion are classified
according to their active site groups in serine-, cysteine-, and aspartic-
endopeptidases. Cysteine- and aspartic-endopeptidases are lysosomal proteins
recruited as digestive enzymes and will be discussed in Chap. 9. Serine
endopeptidases are the most important insect endopeptidases, including the
familiar trypsin and chymotrypsin, and will be detailed in Chap. 4.
Triacylglycerols (fats and oils) are hydrolyzed by triacylglycerol lipases and
phosphatides by phospholipase identified by the link they cleave in the
phosphatide (see Fig. 2.3).
2.4 Phases of Digestion and Their Compartmentalization

in the Midgut
We discussed in the anterior item that digestion may be separated into primary
(or initial), intermediary, and final digestion accomplished by different enzymes.
In this chapter, we will begin to relate the phases of digestion with the gut
compartments to provide a complete picture of the spatial organization of
digestion. We will see that this organization is closely associated with the
phylogenetic position of the insect. Table 2.1 shows that except for the final
digestion of proteins (indicated by a high aminopeptidase activity) that occurs in
the midgut, most digestion is carried out in the crop of Abracris flavolineata
(Polyneoptera: Orthoptera). The participation of the salivary glands is negligible.
As the enzymes are stable in midgut contents along their movement across the
gut, the low enzyme activities recovered in the hindgut indicate they are excreted
at a low rate. This low excretory rate of digestive enzymes is caused by midgut
countercurrent fluxes of fluid. These fluxes move forward enzymes and products
of digestion, as soon they became small enough to pass through PM into the
ectoperitrophic space, thus recovering the enzymes before excretion and
enhancing digestion efficiency. This endo-ectoperitrophic circulation of digestive
enzymes is named enzyme recycling (details in Chap. 6). Secretory and absorptive
regions are qualitatively inferred with the use of non-absorbable dyes, like
amaranth. Secretory regions accumulate dyes injected into the hemolymph on
their hemal side, whereas absorptive regions accumulate dyes on their luminal
side. This will be discussed in detail in Chap. 6. A similar arrangement of the
digestive process was observed in several other Polyneoptera insects (see Chap.
14). It should be remarked that it is not necessary to be functional in enzyme
recycling that the countercurrent flux of fluid occurs from the posterior to the
anterior midgut. It suffices a countercurrent flux taking place from a posterior and
to an anterior site, both in the posterior midgut, as exemplified in detail for the fly
larvae (see Chap. 6).
Among Holometabola, the lower Coleoptera, exemplified by Pheropsophus
aequinoctialis (Coleoptera: Adephaga: Carabidae), the spatial organization of
digestion is similar to Polyneoptera insects (see details in Chap. 14). In higher
Coleoptera, like Tenebrio molitor (Coleoptera: Polyphaga: Tenebrionidae), as they
have no crops, most digestion occurs in midgut contents, with the final digestion
taking place in midgut cells (Table 2.2). As before, the excretion of digestive
enzymes is very low.
Table 2.2 Representative digestive enzymes in midgut compartments of insects pertaining to
three orders
Coleoptera Diptera midgut Lepidoptera midgut

midgut
Enzyme Contents Cells Ecto Endo Cells Ecto Endo Cells
contents contents contents contents
Amylase 94.4 3.8 31.3 39.5 29.2 1.5 (570) 96.7 1.8
(150) (144) (50) (4900) (20)
Trypsin 83.2 9.5 61.8 34.4 (37) 12.4 4.2 (70) 94.5 1.3
(50.5) (4) (200) (0.7)
Acetylglucosaminidase – – 13.5 (79) 6.3 (17) 80.2 36.5 (34) 1.5 62
(31) (0.21) (2.1)
Maltase 95.0 3.6 Trace Trace 88 1.7 (70) 3.4 (20) 94.9
(30) (130)
Carboxypeptidase A – – 17.7(121) 10.4 (54) 71.9 (50) (17) (23)
(150)
Aminopeptidase 10.9 73.0 29.7 13.5 56.8 12.7 7.8 (60) 80
(1348) (465) (700) (700) (150)
Trehalase 72.0 15.3 74.8 24.8 18 – – –
(345) (7.1) (30)
Data according to Terra et al. (1985) (Coleoptera), Terra et al. (1979) (Diptera),
and Ferreira et al. (1994) (Lepidoptera). Figures are % activity of total midgut and
in parentheses are specific activities (mUnits/ mg protein)
Ecto contents ectoperitrophic contents, endo contents endoperitrophic contents; −
not determined
Compartmentalization of digestion in higher Holometabola (Panorpoidea) is

more complicated. This was shown for the first time with the lower Diptera
Rhynchosciatra americana (Sciaridae). When the activities of the digestive
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Attento ouvio Sumano os impios votos;
E hum dos Ministros seos, que jaz mais perto,
Ordem recebe de surgir ao Mundo,
De voar n’hum momento á vasta Eolia,
E dos Tufões ao rispido Tyranno
Taes vozes transmittir:»Que altiva Gente,
»Que indómita Nação, capaz de tudo,
»(Por quem malquisto sempre, e defraudado
»O Reino do pavor carece de almas)
»Sobre Quilha arrogante aparta as ondas,
»Os dominios do equóreo Irmão lhe insulta,
»Que tambem da intenção quer advertido;
»Para que ambos có as forças apostadas,
»No mar cavando, erguendo abysmos, serras,
»O Lenho injusto, audaz sacudão, rompão,
»Que apavóra de Tripoli as muralhas,
»A elle Estygio Rei tão importantes:
»Perdidos os pilotos, e arrancada
»Do alto pégo, ou nas férvidas arêas,
»Ou nas sumidas róchas arrebente:
»Os frémitos do auxilio em vão rogado,
»A festiva Cidade escute, e veja
»Nas aguas os Christãos bebendo a morte.»
Disse, e o Nuncio veloz ao Mundo surge,
Á vasta Eolia vôa, e cumpre o mando.
Já rompem da masmorra os Euros bravos;
Já comsigo arrebatão quanto encontrão
Fóge o molle Favonio, fóge o Dia:
Os campos de Nereo a inchar começão:
Ao longe horrendamente o pégo ronca:
Eis subito encanece, e todo hé montes.
Quasi quasi a cahir d’hum, d’outro lado,
Os mastros vergão, as cavernas rangem:
Qual (se alguem a jogou) saltante péla,
Roça o Pinho os Infernos, roça os Astros;
Vai, e vem vezes cento abaixo, acima.
Carrancudos tres Sóes a luz negárão,
Por tres noites o Céo não teve estrellas:
E se Eólo, em seo impeto afracando,
Deo ao dia segundo algum repouso,
O experto General o ardil penetra:
Á guerra apercebidos chamma, e ferro,
Em tanto que, Neptuno fraudulento,
Tomas serena face; ao alto a prôa
Que se enderece, ordena, assim que os ventos
As vagas sobre as vagas encapellão:
Não succeda, que o pélago fervente,
Os insanos Tufôes contra as arêas
Com hum, com outro embate o lenho atirem.
Então, quanto se dá vigor em Numes,
Na lide porfiosa os dois esmerão:
Em roda novo horror carrega os mares.
Os sanhudos Irmãos guerrêão, berrão,
De regiões oppostas rebentando:
Escarcéos, e escarcéos lá se atropellão:
Por longo espaço treme o fundo aquoso;
Como que está Plutão do Estygio centro
C’os duros hombros abalando a Terra.
De taes, e tantas furias assaltado,
Que arte guiar podia o lenho indócil?
Nem lignea robustez, nem cabos valem:
Cahe com ruidoso estalo a rija antenna,
E batem susurrando as rotas vélas.
Destes gravames nada oppresso em tanto,
Por tudo se divide, a tudo acode,
Todos có a voz, e exemplo aviva o Chefe,
Grassando em todos émula virtude:
Não há frôxos: marêão, saltão, correm.
A engenhosa Prudencia em fim triunfa;
Vence a Constancia audaz; e a largos pannos
Vai-se amarando ovante a Náo veleira.
AQUELLE, CUJO Aceno os Astros móve,
QUE rege o Mar, o Vento, o Mundo, o Averno,
Progresso não permitte á raiva undosa:
E se atê-li soffreo, que encarniçados
Marulhos, Furacões travassem guerra,
Foi para que altamente as memorandas
Forças do Luso peito reluzissem.
Noto, Austro, Boreas, Áquilo emmudecem
Manso, e manso: e, despindo as prenhes nuvens,
O Céo veste hum azul sereno, estreme.
Volve o molle Favonio, volve o Dia,
E volvem mais que d’antes amorosos.
Fôra imposto a Tritão pegar do buzio,
Com que as ondas revoque: o buzio toma;
Surde por entre espumas orvalhoso,
A encher có a voz sonora emtorno os mares.
Eis sópra a concha ingente, e mal que sópra,
Resôa pela Aurora, e pelo Occaso.
Tornão violentas a seo leito as vagas:
Esta recua ás Siculas paragens
Por não vasto caminho; aquella ás Syrtes
Fervendo em rôlos vai; remotas margens
Mais tarde outra revê, donde corrêra
Ao nome, que a attrahio, que á patria sua,
E a Tripoli hé commum: tambem alguma
Foi visinhar có as aguas do Oceano:
Tal que d’antes jámais deixára o fundo,
Ao fundo se desliza, e jaz, e dorme.
Na quarta luz emfim desde as alturas
Tostada Multidão, que lá vigia,
Presume illusa descobrir ao longe
Cadaveres boiantes, vergas, táboas:
Há entre elles alguem, que derramados
Té de Lysia os thesoiros vê nas ondas;
E quem menos de lynce arroga os olhos,
Se atreve a assoalhar, crédulo, insano:
»Que se o pégo poupára algum dos Lusos,
»Só reliquias a Náo desmantelada
»Hia reconduzindo aos patrios lares.»
Mas em quanto delira o Povo adusto,
A gávea se desfaz ao sopro amigo:
Tentão de novo defrontar có as praias,
Que á merecida pena em vão se furtão.
Bem que findasse a noite, o róseo Febo
Não com tudo esmaltava o Mar, e a Terra:
Não era o tempo então nem luz, nem sombra.
Porém como surgio dos Thétios braços
O Filho de Hyperion, e os Céos lustrando,
Com seo raio expulsou de todo as trévas,
Alcança de mais perto, e vê primeiro
Navegante Polaca a véla, e remos,
Que aos Nautas patentêa: o Lenho a segue;
Rápida foge: o remo, o vento a ajudão.
Como no espaço azul medrosa Pomba,
Apenas a Aguia sente, apressa os vôos,
Contra as unhas crueis buscando asylo;
E em seos tremores incapaz de escolha,
De lugar em lugar sem tino adeja,
Por ferinos covis, palacios, bosques,
Assim (quão raramente!) escape ás garras:
De igual modo, apurando as ténues forças,
A curta embarcação, para salvar-se
Do inimigo fatal, varia os bordos:
Mas vendo que evitallo hé vão projecto,
Tomada do receio, a prôa inclina
Á conhecida arêa, e quasi encalha.
Já com menos affronta aqui respira;
Porque os baixios arenosos védão
A tremenda invasão da Lusa Quilha.
Então jactanciosa eleva a frente;
As flamulas no tópe lhe florêão;
Guerra ameaça então, e a guerra chama
Braços, a que a distancia tólhe o raio.
Esta audacia, porém, não fica impune:
Que obsta a Mortaes de espirito arrojado,
Quando iroso calor lhe accende o peito?
Ao Mar leves Bateis subito descem,
E commandados de hum, que os sobrepuja,
Vão có a vingança fulminar o aggravo.
Sobre elles, á porfia, a flor dos Lusos
Enceta heroicamente a grave empresa.
Gentilezas á Fama derão todos;
Todos em feitos grandes se estremárão.
Mas o louvor primeiro a ti compete,
Que d’arvore de Pallas[8] te appellidas,
E cinges vencedor com ella a fronte.
Em saltar ao Batel tu te anticipas,
Tu dos igneos peloiros não detido,
Fórças os remos, a inimiga aferras,
Quando a fusca Equipagem temerosa,
Ao fragil seo baixel picando a amarra,
Nas praias dá com elle, dá comsigo,
E nellas imagina resguardar-se:
Tu primeiro tambem sobre os Contrarios
Disparas férreos globos, que os Cyclópes
Forjárão, fabricando a Jove as armas.
Mais inda remanéce, inda te sobrão
No ensejo Marcial discrimes duros,
Assombrosas acções, que te levantem
Ao cimo de fragoso, aéreo monte,
Lá onde em Paços de oiro a Gloria reina
Com sceptro diamantino, e circumdada
De numerosa, esplendida Assemblêa;
Entre as quaes pela mão da Eternidade
Teo vulto surgirá, marmóreo todo.
Para tanto não basta, que empolgasses
O curvo Bórdo opposto, ou que o subissem
Os Companheiros teos, depois de expulsa
A vil Tripulação por vis terrores.
Os azares, e os jubilos se enlêão,
Por que a mesma desgraça, o que no mundo
Hé mal, hé damno a todos, te aproveite.
Repentina resáca a dois comtigo
Constrange a recuar no débil casco,
E á praia arroja os Tres, quando reflue.
Aqui se vê, qual és, que ardor, que alento
Te abrange o coração, te anima o pulso:
N’hum feito Herculeos feitos escureces,
E quanto as Musas fabulárão delles.
Féra gente, de Arábica linhagem,
De tôrva catadura, hirsuta, e negra,
Pelos serros contiguos vagueando,
Á maneira de lobos, se apascenta
Nas rezes dos rebanhos desgarradas;
Ou, émula do Tigre, as selvas rouba,
Rouba os redis; e o medo, o sangue, a morte
Diffunde aqui, e alli. Munio-se agora
De armas de toda a especie: huns vibrão lanças,
Outros forçosa vara, espadas outros,
Ou pedras, ou punhaes, ou fogo, ou settas.
Ei-los das agras serras vem correndo
Acudir aos Irmãos: (quem há que os conte?
São quaes manadas, que devastão campos.)
Como ardida falange escalar tenta
Castello situado em cume alpestre,
Ou romper torreões de alta Cidade:
Huma, e outra Caterva os Tres investe,
E quanto esforço tem, no attaque emprega.
Se a cada qual dos Tres té-li se oppunhão
Moiros cincoenta, os Árabes, que occorrem,
A cada qual dos Tres oppoem milhares,
Todos bravios, formidaveis todos!
Em que facundia taes portentos cabem?
Quem ha que pasme assás de taes portentos?
Quem, se não fôra testemunha o Mundo,
Por fábula, ou por sonho os não teria?
Trôão da Fama no clamor; e vivem
Olhos, que os virão, braços, que os fizerão.
Era para attentar tão nova scena!
O denodado Heróe, e os Dois, que inflamma,
As bravuras sostem de hum Povo inteiro.
Rue a raivosa, rustica Torrente;
Retumba em valle, e valle a grita horrenda.
D’ambos os lados o Guerreiro apertão:
Sibilão tiros, golpes se redobrão:
Mas elle có a sinistra, elle có a dextra
A Multidão rechaça, illeso, immoto.
Aos Barbaros o pejo atiça as furias:
De artes mil desusadas se refazem
Na espantosa refrega; mas sem fructo:
O Varão permanece invulneravel,
E nas Estygias aguas cem mergulha.
Para aqui, para alli a espada hé raio,
Nunca em vão. D’hum, que audaz de perto o arrosta,
Enterra-a nas entranhas; outro que era
De membros gigantêos, de lança enorme,
E exhortava na frente á guerra os tardos,
A dois golpes, não mais, do Luso Achilles
Jaz inerme; e com hum, com outro arranco
O espirito feroz lhe cahe no Inferno.
A este, que na terra ancioso arqueja,
Vão as auras vitaes desamparando;
Aquelle hé tronco só: por toda a parte
Voão braços, cabeças, fervem mortes.
Ó tu, que dos Almeidas tens o agnome[9],
Tu, que ligar podeste em nó lustroso
Ás honras de Mavorte as de Minerva,
Tambem te faz eterno este aureo Dia.
Se os Lusos, que pelejão sobre as praias,
E aquelles, que a Polaca prisioneira
(Sossobrado o Batel) retem no bojo,
Onde de longe os vexa o Mauro insulto;
Se todos volvem salvos, Obra hé tua.
Em quanto por auxilio a huns, e a outros
Envias Alexandre[10], nunca esquivo
Da nobre estrada, que trilhára o Grande,
Ignivomo canhão, que infatigavel
Respondêra a dezoito bronzeas boccas,
E silencio lhe impôz, de novo esparge
Por entre horrivel som, e opáca nuvem
No centro dos cerrados Africanos
Granizo de lethifera metralha.
O primeiro terror tu lhe infundiste,
Tanto que a de Mafoma agreste chusma
Vio córados de sangue arêas, mares:
O mandado Varão croou a empresa.
Rápidamente o remo as ondas varre:
E Sousa[10] impetuoso aos socios chega:
Contra os donos assésta o bronze adverso,
E assim lhes restitue as férreas balas.
Já cede, já fraquêa a Tropa escura,
De convulso temor enregelada.
Ei-los fugindo vão, nem que aves fossem;
Por huma, e outra parte se tresmalhâo,
Crendo sentir estrépito, que os segue.
A bordo então Donaldo os seus convoca;
Corre a abraçallos, e na voz, na face
O cordial prazer exprime a todos.
Memorando as façanhas huma a huma,
Do condigno louvor as enche, as orna,
Altivo de reger tão brava Gente.
Mal que o descanço os animos sanêa,
(Já declinante o Sol do ethéreo cume)
Á terra se avisinha o mais que póde
A bellicosa Náo; e c’os primeiros
Coriscos Marciaes vareja o Bando,
Que em mór tumulto as praias enxamêa.
Do grande lenho á sombra os lenhos breves,
(Porque estanhado o mar jaz em silencio)
Artes, e forças empenhando, intentão
A Maura presa despegar da margem;
Vãmente, que folgando o lindo Coro
Das filhas de Nerêo, sobre ella salta,
A querem para si, lhe chamão sua.
E quem de hum Nume á Prole, aos seos direitos
No patrio senhorio obstar podéra?
Ou pulsos Briarêos onde acharia,
Para o trabalho immenso? Ella, com tudo,
Nereidas, não foi vossa, indaque dignas
Sois de mil dons, e, como Venus, bellas.
O que á Victoria escapa, engole a chamma;
De jus: damno menor maiores véda;
Mais facilmente detrimentos leves
Caracter pertinaz subjugão, domão,
Do que meigo favor o torna grato.
Arde o Pinho, o furor Vulcáneo reina:
Nutre o pez, e o betume as pingues flammas,
Tanto á pressa, que em vão, inda recentes,
Extinguillas quizera industria humana.
Crebros estalos se ouvem: d’entre o fumo
Brotão centelhas mil, como que aspirão
Ás estrellas volver, donde emanárão.
A lignea contextura eis toda hé fogo;
E o fogo em linguas cento as nuvens lambe.
D’entre penedos, e arvores, que a abrigão,
Ao longo da ribeira a má Progenie,
Accesa em furias vans, o incendio nota:
Cuidadosa de si, da luz não fia;
Artes, porém, que póde, a salvo exerce.
Dalli com mira attenta os Marcios tubos
Huma vez, e outra vez dão som baldado;
Daqui baldados seixos vem zunindo,
Ai! não todos baldados: mão tyranna
Em alvo, que lhe apraz, có a morte acerta:
E aquelles, que a bem custo hum só podérão
Tocar com leve golpe em campo aberto,
Da perfidia amparados, se glorião,
Ao ver que hum semimorto os socios levão.
De Marte a crua Irmã quer este sangue,
Havendo de lavar aos Vencedores
Tudo quanto hé mortal, e dar-lhes vida,
Com que assoberbem as Idades todas.
Silva[11] por isto os séculos invade
Em rápida carreira irresistivel;
França[12] por mãos da Gloria enloira a fronte;
Rocha[13] morrer não sabe; o mesmo ignóra
Esse, a quem de Homem[14] o appellido ajusta;
E o que chamão da Guerra[15], e que o merece:
E tu, claro Avellar[16], com elles vives,
Com elles vivirás, em quanto a Honra
Tiver cultores, e existencia o Mundo:
Ri-se Virtude assim das leis do Fado.
Era o tempo, em que a lassa Natureza
Appetece o repouso; em que os Ethontes
De nectar se robórão; quando a Noite,
Diurnos pesadumes ameigando,
Desdobra sobre a Terra o véo dos Astros.
A quebrantada força então renovão
Os descançados, os jacentes Nautas:
Inda estão repisando o que lidárão.
Este a aquelle refere, aquelle a este,
Que riscos evitára, e que feridas;
E quantos despenhou na sombra eterna.
Fallão huns, outros fallão, té que o somno,
Nunca tão brando, lhe entorpece as linguas.
Mas da fallaz Cidade o Chefe injusto,
De importunos cuidados perseguido,
Os mimos de Morfêo gozar não póde.
Seo negro coração ralão remorsos;
Toma, pela desgraça, o peso ao crime,
Ao crime, indole sua, e seo costume.
O baixel, que perdeo, não dóe ao Féro;
Os mortos Cidadãos tambem não chóra;
Olha sómente a si: já vê, já ouve
As flammas vingadoras; sente o ferro
Ir-lhe sobre a cerviz; escuta o baque
Das muralhas, das torres: pendem, pasmão
Alvedrio, Razão: que escolha há nelle?
»Novamente o Varão, que vezes tantas
»Illudirão traições (diz o Tyranno)
»Emprenderei mover? Submisso rôgo
»Ha de sempre acalmar-lhe as justas iras?
»Se os Francezes lhe der, tão mal negados,
»Será bastante? O que exigia, havendo,
»Não ousará tambem quebrar promessas,
»E no abuso da fé regozijar-se?
»Vingança hé deleitosa ao resentido;
»Sómente se não vinga o que não póde.
»Que, pois? ... Á dubia sorte dos combates
»A mim proprio exporei, e os meos prazeres?
»Dubia disse? ... Tentalla hé perder tudo.
»Se podérão só tres pôr medo a tantos,
»E esses mesmos a vida (oh pasmo! oh pejo!)
»A tantos arrancar, ficando illesos,
»Quem há que lhe resista, unidos todos?
»Fóge, infeliz; e o que podéres, salva;
»Fóge: assim pouparás vergonha, e morte.
»Mas ah! triste! Em que plaga hirei sumir-me?...
»Que mar, ou que paiz, bem que deserto,
»Guarida me dará, prófugo, errante?...
»Quem terei, que me siga, amigo, ou servo,
»Já nua de esplendor minha grandeza?
»Antes vulgo infiel após meos passos
»Bramindo correrá; e ou da existencia,
»Ou dos haveres meos, ou della, e delles
»Por carniceiras maons serei privado.
»Não, não; nossos desastres custem caro;
»Usemos toda a fraude, os crimes todos.
»Cerque-se de traições esse Guerreiro,
»Vaidoso do troféo: có a falsa offerta
»De tudo o que de mim quizer o Avaro,
»Posso aqui outra vez, posso attrahillo.
»E quando imaginária utilidade,
»Vã cobiça o trouxer, se das ciladas
»Intacto apparecer ante meos olhos,
»Em pedaços farei có as mãos, có a bocca
»A nefanda cabeça: ao peito aberto
»O coração maldito hei de arrancar-lhe;
»Roello, devorallo inda fumante.
Tal esbraveja; e nem a si perdôa,
A si labios, e mãos morde, remorde:
Qual hórrida Serpente, encarcerada
Entre férreos varões, se alguem a assanha,
Com rápido furor se desenvolve,
Cem vezes arremete ao que a provoca;
Mas vendo, que debalde exerce a furia,
De sangue os olhos tinge, agudos silvos
D’entre as fauces venéficas despede,
Com que a farpada lingua está vibrando;
Em tudo o que a rodêa, em tudo ferra
Os espumosos dentes, e em si mesma,
Ensovalhando o chão, e a vária cauda
Có as sórdidas peçonhas, que vomita:
Em tanto o mofador se ri seguro.
Da Aurora o nuncio amiudára o canto.
O matutino humor tempéra as mágoas,
E os somnos insinua até no Afflicto:
Por isso do Bachá desatinado
Virtude soporifera se apossa,
Lhe amansa os frenesis, lhe cerra os olhos.
Como quem fatigado está das iras,
Pesadamente o Bárbaro resóna.
A seos males, porém, não colhe allivio,
Nem demorada paz lhe rega os membros.
Fantasmas, que velando o espavorião,
Inda entre a doce languidez o aterrão.
Vê-se indigente, só, desamparado,
Ermos em outro mundo a pé trilhando,
Ermos sem rasto de homem, nem de féra;
Onde ave alguma não discorre os ares.
Já sévo Abutre de implacavel fome
Lhe atassalha as entranhas; já querendo
Fugir de hasta inimiga, que o persegue,
Que lhe toca as espaldas quasi, quasi,
Treme todo, e mover não póde a planta;
Já pende de ardua rócha sobre as ondas.
Eis entre estas visões, que traça o Medo,
Imagem verdadeira, agigantada,
Clara, como o que a luz nos apresenta.
Surge aos olhos do attónito Agareno.
Aquelle a quem venéra ainda o Ganges,
E o rio[17], que Imaús na origem banha;
Aquelle, que de jus noméão Grande,
De Marte émulo não, mas Luso Marte,
Albuquerque immortal, de amor eterno
Pelos seos penhorado, esquece o néctar;
E, escusando hum momento os bens celestes,
Não desdenha baixar aos impios Muros,
Nem có a palavra serenar discordias.
Á Náo, que do seo nome se engrandece[18],
Arde por madurar devidos loiros.
Com vozes ponderosas accommette
O aterrado Tyranno, que maquina
Na desesperação atrocidades.
Resplandece o Guerreiro; hé tal, hé tanto,
Como quando o temeo por vezes duas
A que do Indico Estado hoje hé Cabeça;
Como quando Malaca o vio triunfante;
E em ti, pomposa Ormuz, pendões erguia:
No magestoso olhar, na longa barba
Traz a veneração, e arnez hé todo.
»Que intentas, miseravel? Que revolves
»No espirito dobrado? (a Sombra exclama).
»Crês acaso afastar o mal, que te insta,
»Perfidia com perfidia encadeando?
»Não sabes, por ventura, a quem te atreves?
»Que Nação contra ti, que Throno irritas?
»Esquece-te, que nunca impunes deixão
»Taes crimes? Quem melhor, que Moiros, deve
»De Luso conhecer a ousada Estirpe?
»Inda que até dos teos a historia ignores,
»Força hé que saibas o que sabem todos:
»Que estragos, que deshonras grangeastes
»Deste Povo de Heróes, em resistir-lhe.
»Sobre esmagados collos de Reis Moiros
»O Maior dos AFFONSOS, o Primeiro
»Impoem da Monarquia a Base eterna.
»Flagello assolador da Maura gente,
»Em quanto a Regia Mão fulmina o ferro,
»E o grão Mendo, nas portas entalado,
»Abre caminho aos seos; eis se apodérão
»Da celsa Fortaleza, e da Cidade,
»Que hé longa tradição fundára Ulisses;
»Essa, que do aureo Tejo honrando as margens,
»Alterosa, escorada em sette montes,
»Taes fados mereceo, que ambos os Pólos
»Tiverão de acatar-lhe as Leis sagradas.
»SANCHO, digno do Pai, com quantas mortes
»Injustas possessões ao Moiro arranca,
»E ajunta novo Reino ao Reino Avito!
»Ondas de negro sangue Mauritano
»Pela terra visinha, e pela herdada
»Derramão, coriscando, outros AFFONSOS.
»Nem maculou sómente os nossos campos
»A mortandade vossa. O Quinto AFFONSO,
»E o Primeiro JOAÕ restavão inda,
»QUE ao proprio seio d’Africa levárão
»Ferro, e flamma, e terror: MANOEL restava,
»Feliz, (e com razão Feliz chamado)
»QUE, maior do que o seo, quiz ter mais Mundos,
»E a QUEM prostrados Reis seo REI quizerão.
»Tangere o sabe; Arzilla, e Ceuta o dizem;
»O attestão Indios, Númidas o attestão.
»Relatar huma, e huma acções tamanhas
»Para que? Dos Heróes sómente os nomes,
»Sem o immenso louvor, que os acompanha,
»Pedem horas: sobeja o que hás ouvido,
»Para attentares bem, que lance estreito
»Hé o lance, em que estás, e com que Gente.
»Pondéra ainda mais, quão despresiveis
»São para o Portuguez ciladas tuas:
»Há muito que a experiencia nos ensina
»Até que altura o Moiro enganos sóbe:
»A Prudencia, e Valor nos meos competem.
»Porque, pois, te detens? Supplice, e curvo
»Huma vez, outra vez, porque não rógas
»Aos Lusos teo perdão, bem que indevido?
»Se elles se pagão de calcar soberbas,
»Se de punir delictos se comprazem,
»Apiedar-se do réo tambem lhe he uso,
»Quando os implora. Ao tempo, em que vingado
»O Sol tenha o Zenith, a Náo possante,
»A maior, que teos portos fortalece,
»Será do Vencedor; sello-hão com ella
»Dois menores Baixeis recem-cativos,
»E o Chefe, e as Equipagens numerosas.
»Mas não temas; có a supplica rendida
»Tudo recobrarás. Cobiça de oiro
»Jámais vicia o peito aos generosos:
»Não quer servos, nem presas; quer amigos
»Minha honrada Nação. Eia, aproveita
»O tempo, que te hé dado: olha, que foge.»
Disse, e voou sem que resposta espere.
Salta do leito o Moiro arripiado,
Volve em torno, e revolve os turvos olhos.
Quasi arrombando as portas, corre tudo,
Tudo vê, chama, brada, acodem servos;
Mas não sabe, o que diga, absorto, insano.
Nisto ao mar de repente os olhos volta;
Por todo elle os alonga, e fica immovel.
Em quanto as ondas sôfrego examina,
Não ser sonho a Visão, no effeito observa.
Vê como a Lusa Náo demanda o porto;
Como próxima a elle, em roda vira;
Como enfunada, e mais veloz que os Euros,
Vai dar caça ao Baixel, que ao longe aponta
Com remeira Galé; vê como as toma;
Como as presas conduz, e audaz campêa:
Como sobre a maior em fim subido
Castro[19], e nada tardio, á voz do Chefe,
Outra, que sobrevém, combate, e rende.
Fôra melhor á Triste o dar-se logo.
Daquella, bem que inutil resistencia,
Gloria, afoito Avellar[20], houveste em dobro.
Usado a presumir que a morte hé nada,
Com poucos, e munido de ti mesmo,
Eis o Mauro convés ganhas de hum salto:
Gira o ferro, e triunfas, dois prostrando.
Tudo isto, verdadeiro em demasia,
E d’alta Apparição vaticinado,
Caramáli[21] do Alcáçar descortina.
Primeiro o coração lhe agitão furias;
Não pára; vai, e vem; doudeja, freme;
As melenas arranca, arranca as barbas:
Pouco a pouco depois temor o abranda.
Gravado tem o Heróe na fantasia;
E porque em tudo o mais o vê sincero,
No resto da Visão firma esperanças.
Hesitando, com tudo, em si murmura:
»Quem do contrario seo fiar-se deve?»
Mas, passado hum momento, assim não pensa.
»Em tentar que me vai? Senão, que resta?»
Disse, e a hum, entre os seos authorisado,
Que lhe provára fé n’outros extremos,
Envia de Albuquerque á Náo temida
C’os Francezes fataes, que, á similhança
Da Gorgónea carranca, damnão vistos.
Diz-lhe (se tanto ousar)»que em troco delles
»Peça os Varões, os Lenhos apresados;
»E tudo facilite ao grato assenso.»
Além das esperanças vai o effeito:
De nada para si querendo a posse,
Donaldo restitue (acordes todos)
O Almirante infiel, Varões, e Lenhos;
E prende a tantos dons o dom brilhante,
Que suspira o Bachá, de Amigo o nome,
Promettendo que o Throno há de approvallo.
O coração do Régulo não basta
Ao jubilo insperado. Alegres vivas
A voz dos Cortesãos, e a voz do Povo
Manda aos ares: no pélago reflectem,
E tocão dos Lusiadas o ouvido.
Que nectáreas correntes inundárão
Portuguezes espiritos, olhando
Sobre as amêas das profanas Torres
As Bandeiras de hum DEOS, de CHRISTO as Quinas,
Do Reino occidental eterno Abono!
Em quanto acclamações da infida Plebe,
E a espaços o trovão da artilheria,
Já do mar, já da terra, os Céos atrôão!
Eis de tanto suor o idóneo preço:
Quem seo DEOS, e seo REI a hum tempo serve,
Que mais quer, ou da Gloria, ou da Ventura?
A Ti, ó Lima[22], Conductor supremo
Da Lusitana Esquadra, a Ti, que és Grande
Na Ascendencia de Reis, no Gráo, nos Fados,
Inda maior no Engenho, e na Virtude,
Tambem do Caso illustre se deriva
Applauso não vulgar: por Ti mandado
Fez o patrio Valor tão raras coisas:
Foi sua a execução, Teo fôra o plano.
Nem menores pregões Te deve a Fama,
Nelson preclaro, da Victoria Filho,
Que usurpas a Neptuno o grão Tridente:
O que o Luso acabou, Tu lhe apontaste.
Mas a origem de tudo a quem respeita,
A quem melhor quinhão de gloria cabe,
Ou falle a Musa, ou não, ninguem o ignora:
Soão praias seo nome, e soão mares.
A Nautica Pericia, que afamados
Outróra os Portuguezes fez no Mundo,
Que os levou a reinar a extremas plagas,
Sem cultura jazia (oh vilipendio!)
Do centro das Brasilicas florestas
Desarreigadas quilhas inda arfavão
Sobre as Tágicas ondas, mas em ócio.
E se alguma imprudente ousava acaso
Ás Hyadas expôr-se, expôr-se a Arcturo,
Ronceira dividia o Lago immenso,
Dos mares, e dos ventos esquecida;
Incapaz do Conflicto, e da Procella.
Raro o Nauta, e com alma entorpecida,
O ministerio seo desaprendêra:
Obedecer, mandar nenhum sabia
Eis Coutinho[23]: eis o Genio antigo acorda;
Eis nova Geração com elle assoma.
Para Marte, e Nerêo sábia Académia
Cultiva Cidadãos: escolhe entre elles
O illustrado varaõ, quem se avantaja;
E, bem que repartido em mil cuidados,
O peso de altas coisas sostentando,
C’o louvor afervora o que he louvavel,
E em quem merece o premio, os amontôa:
Desta arte a Mocidade aos astros sóbe;
Assim com Socios taes luzio Donaldo.
Oh tres, e quatro vezes venturosos
Nós, aquém dado foi, que respiremos,
Subditos de JOAÕ, serenas vidas;
E ser de tanto Bem participantes!
JOAÕ, da Patria PAI, RENOVO Insigne
De Monarchas, de Heróes, de Semideoses;
AMOR, GLORIA, ESPERANÇA, e LUZ da Gente,
Que, os mares invadindo, ousou primeira
Ver, e afrontar o Adamastóreo vulto;
Desde a ultima Hesperia hir lá na Aurora
Arvorar contra as tórridas Falanges
O Estandarte dos Céos, Penhor do Imperio;
JOAÕ, QUE em quanto as Guerras tudo abrázão,
Em quanto Erinnys senhorêa o Mundo,
Afaga, Justo, Pio, Optimo, Ingente,
Com amorosa paz os largos Póvos,
Que o Jugo LHE idolatrão, perto, e longe;
Do Exemplo dos AVÓS Illuminado,
D’ELLES nutrindo em SI toda a Virtude,
Na principal, na egregia SE realça
De eleger (tudo o mais daqui depende)
Almas, com quem do Sceptro adoce o peso.
Astuto Cortezão, que ambiciosos,
Sinistros, devorantes pensamentos
Com zelo vão, fallaz pallia, e doira.
Hé por ELLE repulso; e chama aquelles,
Que as Honras merecendo, ás Honras fógem.
O veneno dos Paços, a Lisonja
Ante Seos Olhos em silencio treme:
Só da Verdade Oráculos attende,
Só da Sciencia Oráculos escuta:
Pallas, Themis presidem-LHE aos Conselhos;
Ás Acções LHE presidem Themis, Pallas.
Não, para sobjugar Nações, Imperios,
Não despe o ferro aqui Gradivo iroso;
Mas só porque na força a Paz se estêe
E só porque sem nódoa permaneção
O Decóro, os Brazões de altos Maiores.
Não he Seo, para SI JOAÕ não reina:
O Pôvo, a que dá Leis, prefere a tudo.
Orem Nobre, Plebêo, Nautas, Colonos,
Ou diante do Solio, ou não presentes;
Ore o Commerciante, ore o Soldado;
Provão merecimento? Os premios levão.
Volve feliz o que infeliz O busca:
A todos satisfaz, Igual com todos;
E até mesmo ao desejo o Dom precede:
Só com pesado pé se móve a Pena.
Ó Lysia, ó Patria, surge, altêa a fronte:
Que não cumpre esperar com taes Auspicios?
Eia, applaude a Ti mesma, ó Lysia, applaude.
As Tres, em cuja voz os Fados soão,
Prazeres de oiro para Ti já fião.
Sahe, (Reinando JOAÕ) sahe das estrellas
Ordem nova de Séculos ao Mundo:
Folga: Assombros tens já; viráõ Portentos.
Sôltas do coração, mil preces manda
Aos Climas immortaes; fatiga os NUMES,
Porque da ESPOSA ao lado Excelsa, e Cara
O CONSORTE Real no Throno exulte;
Porque orvalho do Céo fecunde, amime
Os Tempos de JOAÕ, de nuvens limpos;
Porque IDOLO dos Seos, TERROR de Estranhos,
Brilhe, viva, e dos Netos Netos veja;
Até que tardas Eras O arrebatem
Aos Astros, donde veio honrar a Terra:
ELLE hé digno de Ti, Tu digna d’ELLE.
FIM.
NOTAS DE RODAPÉ:
[1] A Cidade de Tripoli na Barbaria.
[2] O Bachá de Tripoli José Caramali.
[3] O Chefe de Divisão Donald Campbell.
[4] ElRei de Hespanha.
[5] O Grão Turco, a quem hé subordinado o Bachá.
[6] Carlos XII. de Suecia.

Molecular Physiology and Evolution of Insect Digestive Systems Walter R Terra Clelia Ferreira Carlos P Silva

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Molecular Physiology and Evolution of Insect Digestive Systems Walter R Terra Clelia Ferreira Carlos P Silva

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Molecular Physiology and Evolution of

Insect Digestive Systems Walter R

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ISSN 2405-853X e-ISSN 2405-8548

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2.2 Gut Morphology

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Coleoptera Diptera midgut Lepidoptera midgut

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