Anllu. Rev. E7IIO/llol. 1995. 40:85-103

EXTRA-ORAL DIGESTION IN

PREDACEOUS TERRESTRIAL

ARTHROPODAl

Allen Carson Cohen USDA Agricultural Research Service, Western Cotton Research Laboratory,

Phoenix, Arizona 85040

KEY WORDS: digestive biochemistry, feeding ecology, evolution of feeding, mouthpart morphology, predator behavior

ABSTRACT

At least 79% of predaceous land-dwelling arthropods use extra-oral digestion (EOD) as a means of utilizing relatively large prey with intractable cuticles. Through the injection of potent hydrolytic enzymes, either by refluxing or nonrefluxing application, these predators greatly increase the efficiency of prey extraction and nutrient concentration. The advantages of EOD are expressed ecologically as an abbreviation of handling time and an increase in the nutrient density of consumed food, allowing small predators to consume relatively large prey. The basis of EOD is a highly coordinated combination of biochemical, morphological, and behavioral adaptations that vary with different taxa.

OVERVIEW

Extra-oral digestion (EOD) constitutes the chemical pretreatment of food that enhances its nutrient quality or accessibility. This strategy, which is widely distributed in Animaiia, usually involves liquid-feeding and is used in many feeding niches. EOD does not entail ingestion of materials that preexist as liquids (such as hemolymph); rather, it is the digestive liquefaction of solids and reduction of viscosity of intractable liquids.

IThe US Government reserves the right to retain a nonexclusive, royalty-free licence in and to any copyright covering this paper. Mention of a tradename or product does not constitute endorsement by the USDA.

8S

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

86 COHEN

The concept of EOD (extraintestinal, external, preoral, or extracorporeal digestion) was recognized as early as 1910 by Jordan (49). By 1924, many kinds of animals besides arthropods were known to use EOD (60). The behav­ior is present in 12 out of 30 invertebrate phyla-Protozoa, Platyhelminthes, Rhynchocoela, Rotifera, Nematoda, Annelida, Mollusca, Arthropoda, Onycho­ph ora, Pogonophora, Sipuncula, and Echinodermata (6)-i.e. nearly every phylum containing predators. Although EOD has long been recognized as a digestive strategy, little attention has focused directly on the subject. The practice is ecologically important because it allows relatively small predators to use large prey that cannot be swallowed whole or ingested piecemeal.

In EOD, disgorged secretions and the mechanical actions of mouthparts liquify the contents of prey, dissolving nutrients and forming lipid micelles or small particles (22, 33). Arthropods use two types of digestive pretreatment: (a) type I EOD, the chemical liquefaction of prey performed entirely within the prey's body, which in effect turns the prey's exoskeleton into an extension of the predator's gut (89), or (b) type II EOD, the mechanical disassembly of prey and chemical digestion of the nutrient-rich components within a region outside the predator's mouth but within the sphere of its mouthparts (Table 1).

Table 1 Distribution of extra-oral digestion in Arthropoda"

Subphylumla Class Ordersb TypeC

Chelicerata Arachnida Scorpiones (717) II Pseudoscorpiones (18/18) II Solifugae (12/12) II Uropygi (5/5) II Amblypygi (4/4) II Araneae (51/51) IR and II Acari (24124) IN and II Opiliones (0/15)

Mandibulata Chilopoda All families (9/9) I? and II Insecta Thysanoptera (2/2) I?

Hemiptera (29/29) IN Neuroptera (11115) IR + N Mecoptera (III) I? Coleoptera (12/17) IR and II Diptera (7/13) I? and II Dennaptera (0/2)

Orthoptera (0/1)

Odonata (0/11)

"References: 5, 10,29,30,33,48,61,65,66,67,86,93,98. ·Parentheses enclose the numbers of families reported to use EOD in relation to the total number

of families known to contain predaceous members in the order. CIn type I EOD, enzymes are injected into the prey where liquifaction takes place in an otherwise

intact body covering (exoskeleton cuticle). In type II EOD, the prey is cut or torn into smaller pieces that are carried to a preoral region of the mouthparts. N, Nonrefluxers; R, refluxers.

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 87

The former type of EOD is found throughout Arthropoda while the latter is found in several of the Chelicerata and in some Mandibulata (Table 1).

Predators using type I EOD can be further divided into nonrejluxers, i.e. species that use a one-way flow of digestive enzymes, and rejluxers, which repeatedly pump enzymes in and out of prey. In the former (e.g. true bugs), enzymes are produced in specialized glands, pumped into the prey, and in­gested into the predator's gut where they remain until digestion is complete. In the latter (e.g. spiders and beetles), the enzymes originate in the gut and are repeatedly pumped into prey and back into the gut. Nonrefluxers are limited by the amount of enzyme they can produce within a given time frame, while refluxers can continuously feed on a single or mUltiple prey with only negli­gible loss of enzyme activity. These two strategies have a major influence on the ecological potential of predators, as discussed below.

EOD is a cyclical and incremental process. After prey is subdued, a series of injections of digestive fluids is followed by ingestion of the disgorged fluids and portions of the liquified prey (1, 5, 22, 23, 33). This cycling and incre­mental feeding increases the efficiency of the digestive process by maximizing the concentrations of hydrolytic enzymes in proportion to the volume of prey to be liquified. It also maximizes the surface area of contact between the enzymes and as yet undigested substrates. The universality of this cyclical/in­cremental feeding across taxa indicates that the process has evolved inde­pendently many times and testifies to the efficacy of this strategy (20, 21).

ECOLOGICAL AND BEHAVIORAL BASIS OF EOD

The rich availability of terrestrial arthropods in terms of numbers, biomass, and broad ecological distribution (104) makes this group an excellent target for predators. Tropical, terrestrial arthropods occur in a normal size distribu­tion; most species range from about 1 to 10 mm in length (27, 83), providing a bountiful ecological opportunity for predators that can utilize arthropod prey of this size. Furthermore, the nutrient composition of arthropods is rich, char­acterized by protein- and lipid-dense profiles (21, 22).

The marginal value theorem (15), however, predicts that successful expan­sion into a new niche requires that the reward from a new food type must exceed expenditures in the acquisition of that food. In the case of predation, these energy and material expenditures are allocated to search, pursuit, sub­duing, handling, and processing (45, 46, 85). Predators of terrestrial arthropods must gain adequate nutrient reward from prey that range from about 1 Jlg to about 50 g (27) and that are surrounded by a formidable cuticular barrier (36, 90). Individuals weighing less than 1 g compose the majority of arthropod biomass (27), and a large portion of the prey's mass may consist of cuticle, a generally inaccessible barrier (36, 90). Predators that ingest only the internal

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

88 COHEN

contents of their prey have the advantage of selecting nutrient-rich food un­burdened by indigestible and potentially damaging cuticular structures (20-23, 27,43).

EOD as a Method of Food Preparation and Expansion of Predatory Scope

Prey preparation, which takes many forms in the animal kingdom, allows a relatively small predator to consume prey too large for its gape (21, 52). Predators such as birds or bats cull the legs, antennae, and other sprawling parts from arthropod prey, thereby limiting themselves to tissues with higher nutrient value and increasing the net amount of prey ingested (52). Use of venoms, another form of prey preparation, has evolved in at least five families of snakes, a family of lizards (34), and many invertebrates (6). Such preparation expands the predatory scope, or the effective size range of prey that can be exploited (21, 22, 43). Importantly, while EOD increases the maximum size of prey that a given sized predator can handle, it does not compromise the predator's ability to handle prey at the smaller end of its prey range. Con­versely, an increase in gape size or predator size would restrict the smaller end of the prey-handling scope during both the evolution of the modification and afterwards (84).

Modifications increasing body size as a means of extending prey range often impose serious ecological and metabolic limitations, but the use of EOD renders such increases unnecessary. In fact, arthropod predators using EOD tend to be in the moderate to smaller size range, with the exception of some belostomatids, centipedes, scorpions, spiders, and vinegaroons-all of which regularly use vertcbrate prey (10, 33, 93).

The Cyclical Nature of EOD

EOD is a cyclical process consisting of three phases: (a) injection of venoms andlor digestive enzymes, (b) pause or mechanical action, and (c) ingestion of liquified material (I, 3, 22, 23, 38, 39, 64). This cycle is repeated so that the liqucfaction and removal of prey contents are incremental. An important aspect of this behavior is the recovery of both the prey contents and the digestive enzymes that were invested in the prey. In carabid beetles, the recovery of disgorged enzymes was over 70% in natural prey but less than 50% in horse meat (16). Recovery of the digestive secretions is necessary because disgorged digestive enzymes are important in lumenal digestion once they are reingested (23); loss of these secretions also means forfeiture of nutrients because the digestive fluids are mixed with liquified prey contents; and digestive secretions represent a significant portion of the predator's total protein pool, e.g. at least 3.5-5.0% of the total protein in spiders (77). Loss of digestive enzymes caused

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 89

by leakage or interruption of the feeding process can be extremely costly to EOD-using predators, especially refluxers.

Partial Consumption

Often, predators abandon prey before fully utilizing it. Such partial consump­tion (PC) influences the functional responses of predators in their ecosystems, including attack rate, handling time, and predator/prey size ratios (28, 42, 45, 46, 63, 64). In discussions of PC, prey are considered resource patches.

The occurrence of PC has generated two paradigms: (a) proximate or mecha­nistic models (64) and (b) deterministic models (63, 64). The former are based on physiological constraints such as gut capacity or digestive rate limitations, the latter on optimal foraging or the marginal value theorem. Empirical evi­dence supports both the proximate (28, 35, 38) and the deterministic model (3,15, 96); therefore these models may not be mutually exclusive (63, 64).

Although EOD-using arthropods have served as the subjects of most studies of PC (3, 64), no attention has been paid to how EOD influences abandonment of prey patches. Among EOD-users, refluxers are more apt to move on to new patches of prey without a pause for refurbishment of enzymes (3, 22, 38, 39). For example, coccinelid larvae used at least 30 EOD cycles in consuming each prey aphid (1). Evidently, in many of the species that use EOD, there is a finely tuned interplay between the application and removal of digestive en­zymes and the overall efficiency of prey utilization. Whether the predator is a nonrefluxer or refluxer will have a strong impact on the PC decision-making process. The enzymes are an indispensable resource that must be given appro­priate time to liquify prey and must be recovered for further use in the gut if the predator is to exploit their full value. Moreover, the enzymes cannot be immediately replaced should they be misspent (5, 22).

Although some predators can increase extraction rates in correlation with prey numbers (3, 35), many EOD-using predators must invest so much of their resource enzymes and venoms in the initial phases of EOD that moving on to a new prey item before fully utilizing the current one seems unprofitable (19-21). Strong correlations between enzyme kinetics and extraction rates, extraction efficiencies, and enzyme recovery (16, 23, 55) make it imperative to consider the influence of EOD before interpreting PC.

Studies of PC and optimal foraging strategies often proceed under the assumption that all the extractable parts of the prey are of equal value, generally in terms of energy reward (25, 63, 64). However, I have found in studies with Hemiptera that the proportions of different nutrients extracted during the first third of the feeding cycle are different from those extracted in later stages; proteins and glycogen are generally taken early and lipids are ingested late in the feeding bout (Figure 1). Because nutrients are not homogeneously extracted from prey, assessments of optimal foraging as a determinant of PC must

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

90 COHEN

NUTRIENT LA YERS Prey Nutrient Content During Feeding

Minutes After Onset of Feeding

Figure 1 Nutrient extraction from Spodopfera exigua larvae by Zelus renardii during different time periods of feeding. Most of the extractable proteins and glycogen are removed during the first 4S min, but extraction of lipids requires 90 to 13S min. These differences in extractability can be considered as nutrient layers, with lipids being the most inaccessible or the deepest layer.

account for nonuniform nutrient reward. The assessments should be sensitive

to the EOD-related time and nutrient quality differences in the extraction capabilities of various predator species.

Such differences are evident in Figure 2, which shows that representatives from families from two different phylogenetic lines of predators have markedly

different EOD kinetics. Cimicomorphs have a much longer history of predation (18, 19) and much higher rates of protein digestion than do pentatomomorphs. These differences account for large discrepancies in the handling time and extraction rates of members of the two groups (AC Cohen, in preparation). Optimal foraging strategies in these two phylogenetic lines are strongly im­

pacted by digestive rates and handling times.

REQUIREMENTS FOR EOD

Digestive enzymes are nearly universal in Animalia, but a means of delivering them efficiently to an external food source requires special modifications. The source of the digestive enzymes may be specialized structures, such as max­illary or salivary glands found. in many insects and mites, or the gut, as in spiders and some beetles (30, 33, 98). The system for delivery of digestive

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

1400

- 1200 � c a 1000 ..... .;t

'E Q) 800 (.) c ctI

.0 600 ..... 0 If) .0 � 400 w -..J I- 200

0 0 15 30

EXTRA-ORAL DIGESTION 91

45 60 75

Time (Minutes) 90 105 120

I-+- Cimicomorphs --8- Pentatomomorphs

Figure 2 Kinetics of a trypsin-like proteinase from two species (from the order Heteroptera) of

Cimicomorpha (Zelus renardii and Sillea con/lisa) and two species of Pentatomomorpha (PodislIs mQculiventris and Elithyrhynchlls j1oridalllls) measured by hydrolysis of benzoyl-DL­arginine-p-nitroanilide (BApNA) as described in Ref. 23. The rate of protein hydrolysis in the cimicomorphs is much higher than that of the pentatomomorphs, an observation in concert with handling times and prey extraction rates.

juices and for the uptake of Iiquified nutrients may comprise slightly modified chewing mouthparts, or it may consist of specialized mouthparts such as sty lets, forceps, or other hypodermic-like devices. EOD-using arthropods have filter­ing systems composed of hairs (scorpions and uropygids), rasp-like plates (some spiders) (33), or narrow-diameter tubes (hemipterans, some coleopter­ans, and neuropterans) (29, 67, 98). These filters guard against entry of large (> 1.0 !lm) particles into the true digestive tract. Often the filters must be backwashed with an antiperistalsis of liquids from the gut (33).

Many arthropods that practice EOD use venoms to debilitate or kill their prey (spiders, scorpions, ant lions, some heteropterans), but venoms do not occur universally in EOD-using arthropods (uropygids, solifugids, some bee­tles, some heteropterans). The biochemical differences between venoms and digestive secretions are difficult to resolve, especially since many venoms originate from digestive-system structures (94).

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

92 COHEN

BIOCHEMICAL BASIS OF EOD

The fundamental nature of digestion is to render macromolecules into simple compounds that can be absorbed and circulated (36, 47). The digestive enzymes

are alI hydrolases (4), including proteinases, lipases, carbohydrases, and nu­

cleases (36, 47). Proteinases probably are the most important liquefaction enzymes for predators (23, 70, 92).

The proteinases are classified as endopeptidases and exopeptidases (23, 58).

Endopeptidases attack protein molecules from within, reducing insoluble struc­

tures into water-soluble subunits. Trypsin-like enzymes (TLE) attack proteins at their basic amino acid sites, cleaving the proteins at lysine and arginine residues (23, 58). Chymotrypsin-like enzymes (CLE) attack proteins at their

aromatic sites. Both TLE and CLE operate at basic or neutral pH (22, 23, 36,

58). Other proteinases such as pepsins, cathepsins, and thiol-proteinases have been found in the gut of many arthropods, but have not been reported from

EOD secretions (23, 58). The digestive secretions of several species, especially heteropterans, contain TLE (22, 23, 91, 92), and many studies have shown that

this protein is a salivary enzyme. However, CLE has not been reported from salivary secretions (23). Of the exopeptidases, neither aminopeptidases (which cleave amino acids from the amino-terminal end of peptides) nor carboxypep­tidases (which cleave amino acids from the carboxy-terminal end of peptides) are found in the saliva of heteropterans (23). Digestive fluids from spiders had TLE, CLE, carboxypeptidase, and aminopeptidase activities (77). This com­plete compliment of endopeptidases and exopeptidases is to be expected from EOD-using arthropods whose digestive enzymes all originate from the gut

rather than salivary glands. Therefore, refluxers use in their EOD more diverse

digestive enzymes than do nonrefluxers. Triacylglyceral lipases (TAG) were found in the saliva of heteropteran

predators (22, 103), whereas phospholipase A2 (PLA) was detected in heterop­tcran saliva (22, 26) and in spiders (79). TAG digests storage lipids localized in the fat body and reproductive systems of prey. PLA digests the phospholipids in cel\ membranes, disrupting neurons and muscle celIs (94). These enzymes il\ustrate the difficulty in resolving differences between digestion and en­venomation (26, 33, 94). Many lipases require at least partial emulsification of the lipid substrates (99a), but no studies have tried to demonstrate the

presence of emulsifying agents in EOD fluids from arthropods. Several preda­tors, including centipedes (61), spiders (80, 84), and heteropterans (22), pro­duce amylases in their EOD secretions. Amylases may be useful in the digestion of glycogen. Both ribonuclease and deoxyribonuclease have been found in the salivary secretions of a hemipterous insect and a spider (79, 92; AC Cohen, unpublished information).

Insects contain considerable amounts of proteoglycans, glycosaminogly-

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 93

cans, chondroitin sulfates, dermatan sulfates, and hyaluronic acids that form connective tissues, basement membranes, peritrophic matrices, and col­lagenous and fibrous tissues (17). Although EOD secretions could reasonably be expected to contain hydrolases that digest these substances, only hyaluroni­dases have been found (26, 78, 92). Hyaluronidase is also a spreading factor for venoms (26, 33, 77, 94). For instance, the saliva of a hemipterous insect separates cells in intact tissue and reduces viscosity of hyaluronic acid and prey fluids (26).

Next to cellulose, chitin is the most abundant polysaccharide found in nature (90). Arthropod cuticles contain 20-55% chitin cross-linked with protein (14,

103), which represents a considerable biomass, but this tissue is unavailable to most arthropod predators, which generally lack chitinase (36, 81, 90). The absence of chitinolytic digestive enzymes might be explained by the fact that most feeding structures are cuticular (14, 33, 103).

MOR PHOLOGICAL AND HISTOLOGICAL ASPECTS OFEOD

EOD is found in several arthropod classes and many orders with diverse mouthparts and digestive glands. Throughout the Chelicerata, the feeding structures are the chelicerae (claws), appendages with a remarkable diversity

of size, shape, dentition, mobility, and adeptness at manipulating prey. A

common feature in Chelicerata is a network of filtering hairs or plates that prevent large, intractable food pieces from being ingested into the gut where

they could possibly cause damage.

The ancestral mouthparts of Mandibulata are of the orthopteroid chewing type (67, 98). Clearly, Thysanoptera, Heteroptera, Neuroptera, Diptera, and Coleoptera exhibit obvious departures from the orthopteroid pattern. In these orders, various mouthparts have become modified for piercing prey, delivering

venoms or digestive secretions, and removing liquified prey substances. The histology of salivary glands of several species of hemipteran predators

(5) and the gut cellular morphology of spidcrs (33) show evidence of a gradual

release of digestive enzymes via a holocrine system that progresses throughout

the course of prey handling. At the end of the feeding process, when the prey

remnants are released, the holocrine cells appear to be completely depleted (5,

36; AC Cohen, unpublished observation). Several hours pass before replace­ment of the discharged cells begins (5, 33), and complete reestablishment of digestive enzymes requires up to two days in heteropteran predators (5). Although this type of histological/ultrastructural evidence of feeding prepar­edness is sparse and deserves further attention, it points to the severe limitations imposed upon arthropods that use EOD as to how readily they should abandon partially eaten prey and attack new prey items.

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

94 COHEN

PHYLOGENETIC SURVEY OF EOD

EOD is the predominant feeding mechanism in predatory Arthropoda. Of 244 families of predaceous arthropods, 192 (79%) have at least some members that use EOD. In the Arachnida, only the Opiliones and possibly a few Acarina do not use EOD; the remaining 121 of 136 predaceous families do (89%). In the Mandibulata, at least 71 of 108 (66%) of the families that include predators have members that use EOD. However, accounts of feeding behavior are often sketchy and are lacking for many species of predators; therefore, these numbers are undoubtedly underestimates.

EOD has apparently evolved convergently at least 24 times, as judged by the different morphological and biochemical natures of the EOD apparatus in Arthropoda and the taxonomic distance between groups where it occurs. This estimate is based on the assumption that EOD was the ancestral condition for Arachnida and that it evolved de novo at least once each in Chilopoda,

Thysanoptera, Heteroptera, Neuroptera, and Mecoptera; 12 times in Coleop­tera; and 7 times in Diptera. For example, EOD is found in coleopterous predators of the two suborders Adephaga and Polyphaga and five superfamilies of the latter suborder (Staphylinoidea, Hydrophiloidea, Cantharoidea, Cleroidea, and Cucujoidea).

Chelicerata

SCORPIONES Like most arachnids, scorpions use chelicerae to tear prey into pieces, which then are placed into the preoral cavity where disgorged secretions from the digestive tract and cecal glands liquify the material (68). The delivery of these fluids is enhanced by a system of channels in the coxae of the pedipalps and coxapophyses of walking legs I and II (68). The cuticular structures and other indigestible materials are held within the preoral cavity while the diges­tive fluids attack the nutrient-containing tissues. The liquified nutrients are strained through the setae of the posterior portion of the preoral chamber, and the remaining intractable material is wadded into a mass that is expelled.

ARANEAE Like the scorpions, spiders are highly successful EOD predators. They use their chelicerae to manipulate prey as well as to envenom ate them (33). After envenomation, the prey is either chewed by the chelicerae, or it is punctured by these appendages and alternately injected with digestive secre­tions (from the gut) and sucked. In both types of feeding (type I and type II EOD), digestive secretions are mixed with the internal contents of the prey and recovered with the help of the maxillae, labium, rostrum, and pedipalps. The maxillae are modified in the more advanced spiders (Labidognatha) into a saw-like structure (the serrula) and filtering hairs. Further filtering takes place within the pharynx where all solid matter in excess of 1 11m is strained and

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 95

then washed out by digestive fluids (33, 108). Spiders use endopeptidases, exopeptidases, lipases, esterases, chitinolases, and a-amylase in their digestive secretions (77-80). Cheliceral glands produce proteinases and phospholipases that should probably be regarded as venoms rather than digestive enzymes (40,

51,69).

The nature of internal digestion in spiders strongly influences our interpre­tation of how many arachnids use EOD. The midgut articulates with the sucking stomach and branches into a highly complex series of diverticulae that reach into the legs and throughout the prosoma (33). The diverticulae consist of secretory and absorptive cells (71-73).

The complexity of the diverticulae has long been noted (72, 73, 87), but the purpose for this feature is unknown. The midgut is the source of digestive enzymes, the reservoir for ingested prey, and the site of nutrient absorption; hence, to mix incoming food with disgorged digestive enzymes during the gradual process of prey digestion and ingestion seems disadvantageous because the enzymes would be diluted. Compartmentalization of ingested material in diverticulae separate from those secreting hydrolytic enzymes would circum­vent the problem of enzyme dilution.

ACARI Several orders of predatory or parasitic mites use EOD, but this type of prey preparation may not be universal among acarines (30). Of the seven

orders, the Mesostigmata and Prostigmata are strongly predaceous (30). The ixodids are all external parasites of vertebrate hosts and obligate hematophages. Generally, the predaceous acarines insert their chelicerae into the prey, tearing pieces and placing them onto the hypostome where fluids either from salivary glands or the digestive tract are disgorged onto the partially masticated food (30). Morphological adaptations for EOD in Acarina are well-documented, especially in adaptations of the chelicerae for piercing prey (30). In contrast with spiders and scorpions whose EOD enzymes originate from the midgut, some predatory mites use salivary secretions to liquefy prey (59). The presence of salivary glands is widespread in predaceous acarines, but only oribatids (105) and mesostigmatids (30, 31) have been directly shown to use salivary secretions for EOD. The massive salivary styli are prominent adaptations for EOD in predaceous mesostigmatid acarines (30). The biochemistry of the salivary secretions of the predaceous acarines has not been described, and only Ixodida salivary secretions have been studied in detail (30).

Several other arachnids use EOD, but their feeding biology has received little attention (93). These include the whip scorpions (Uropygi), whip spiders (Amblypygi), false scorpions (Pseudoscorpiones), and the wind scorpions (Solifugae) (93). Whip scorpion and whip spider feeding strategies are similar to those of the true scorpions. Chelicerae reach into the prey, tear out pieces and deliver them to the preoral cavity where they are digested with disgorged

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

96 COHEN

gut fluids (AC Cohen, unpublished observation). The harvestmen (Opiliones) do not use EOD (93).

Mandibulata

CHILOPODA Within Mandibulata, the centipedes constitute one of the most consistently predaceous classes, although they have been observed to consume diverse foods (61). Despite some minor feeding differences noted in Scutig­eromorpha, Lithobiomorpha, Scolopendromorpha, and Geophilomorpha, their similarities are sufficient for a generalized treatment here. Feeding begins with envenomation of prey with the poison claws, sometimes by means of repeated chewing by these venom delivery organs. Thereafter, with smaller prey, the entire body is chewed and eaten. Larger prey are bitten, and the centipede then inserts its head into the gaps and disgorges digestive fluids. Published reports differ as to whether centipedes consume solid food or only predigested liquids (55, 61, 65, 66). However, studies of several species whose gut contents contained cuticular fragments (61) indicate that ingestion of solid food occurs in many if not all centipedes. The anatomical source of the digestive enzymes and their biochemical character remain vague (61). Moreover, reports of rela­tively large prey consumed by centipedes, including mice, lizards, toads, and snakes (61), point to some very interesting feeding biology that merits further study.

INSECTA Heteroptera The heteropterans and homopterans have evolved an intricate feeding apparatus (18, 22, 37). The morphological structures include the labium, labrum, and the four sty lets-two inner, interlocking maxillary stylets and two outer mandibular stylets (18, 22, 32, 67, 97-99). The maxillary sty lets form a food canal and a separate salivary canal. The mandibular sty lets are usually the shorter of the stylet bundle, and they are armed with teeth or rasps that (a) initiate penetration of the stylet bundle, (b) grasp the prey in a harpoon fashion, and (c) mechanically disrupt the prey with a rasping action. The styIets are cuticular structures that have mechanoreceptors with extensive dendrites (2) and an ability to twist more than 3600 and bend back upon themselves. In general, they show a remarkable range of movement and dex­terity. They are moved by muscles in the head and are partially controlled or guided by the labium and labrum (18, 22, 98,100,101). While the stylet bundle is moved throughout the body cavity of the prey, penetrating legs, antennae, eyes, cerci, etc, it tears the tissues mechanically and delivers digestive enzymes that mix with the prey tissues (53, 91). The insects alternately pump the potent hydrolytic saliva and suck the liquified prey parts, delivering the nutrients to the digestive tract (22, 23).

The synchronization of morphological, behavioral, and physiological fea-

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 97

tures (including spectacular biomechanical performance, highly potent enzyme activities, and intricate chemo- and proprioreception coordination as well as other behavioral complexities) culminate in an ingestion efficiency of over 94% of the nutrients present in the prey's carcass. Throughout feeding, the inert body wall of the prey remains intact (20). The efficiency of this feeding apparatus is even more evident when one considers that heteropteran predators commonly feed on prey equal or up to five times their own body weight (22, 23), and they accomplish this in about two hours. The digestive enzymes not only mobilize otherwise intractable nutrients, but also reduce the viscosity of the liquids, which must be moved through a feeding canal that is nearly the length of the predator's body and only about 10-15 !lm in diameter (22, 26). Such movement is under the constraints of Poiseuille's principle, which pre­dicts that the viscosity of the fluid, the length of the tube, and especially the diameter of the tube govern the pressure differences required for flow (54, 76). The negative pressures that must be generated by predatory Heteroptera are probably at least as great as those required by blood-feeders, which are esti­mated to be more than two atmospheres (7).

The movement of sty lets in Heteroptera and Homoptera was first described in 1928 (100, 10 1); however, the range of movement, flexibility, and alacrity of the sty lets inside prey (22) suggest that the biomechanics are far more complex and intricate than current accounts allow. Also, the neurobiology of fceding, especially with respect to the sensory and motor feedback mecha­nisms, deserves further attention. Finally, heteropterans and homopterans have long been postulated to be able to inject salivas with different enzyme com­positions, depending on the immediately available substrates (70). This issue deserves further attention, especially in light of the controversies over PC of prey and the ecological and nutritional implications therein.

Neuroptera EOD is practiced widely by neuropteran larvae. They insert sickle-shaped forceps (55) into prey and then pump in digestive juices dis­gorged from the gut (55). The enzyme delivery system is a combination of mandibular and maxillary structures that form each of the two sickles or forceps, which also serve to take up food (13, 62). Although neuropteran larvae undoubtedly have potent digestive enzymes, the digestive chemistry of these impressive predators is unknown.

The mouthparts of most Neuroptera are generalized as the orthopteroid type, but in some important exceptions highly modified structures are elaborately adapted to EOD (67, 98). The enzyme delivery and sucking organs of larval Myrmeleontidae consist of a mandible and a part of the maxilla (11, 67, 106). These structures, also called stylets (67), contain a narrow poison canal and a larger food canal. The food canal empties into a precibarial sack (11, 106). Whether the sack separates the injected and the ingested materials is not clear.

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

98 COHEN

Other neuropteran families reported to have similar feeding structures are the Hemerobiidae, Mantispidae, Sisyridae, Coniopterydigae, and Chrysopidae (67).

Coleoptera Many predatory beetles use EOD, and the use of powerful diges­tive enzymes that are disgorged into the prey's body is especially common among larval predators such as dyticsids, carabids, coccinelids, staphylinids, cantharids, gyrinids, and hydrophilids (29). In several families of beetles, the mandibles of larvae are modified into sickle-shaped and hollowed or grooved structures for delivery of digestive juices (12, 98). The best-characterized use of EOD in Coleoptera is in Carabidae and in Coccinelidae.

The carabids' use of EOD has been the subject of several studies showing the role of enzymes disgorged from the digestive tract and the reingestion of the enzymes and the digested food (49, 74, 75, 82). Not all members of Carabini and Cychrini use EOD despite the fact that the members of each tribe are nearly exclusively carnivorous (16). The principal proteolytic enzyme from several carabids is a TLE, with a molecular weight of 17,800 (16).

The carabids in one study (16) recovered prey proteins with an efficiency of 84%. However, they recovered less than 50% of the proteins and their digestive enzymes from meat. Thus, the feeding system seems adapted to use the prey's exoskeleton as an extension of the predator's digestive tract (22, 23, 88, 89). Efficient recovery of digestive enzymes and nutrients requires an intact exoskeleton of the prey for use as a compartment for the digestive enzymes. This finding raises questions of how predators seal the nexus between their functional mouths and the prey's cuticle. A seal of some sort must be made, especially when liquids are moved between predator and prey under pressure (22, 23, 70).

One of the most compelling arguments in favor of the EOD's relationship to the relative size ratio of predator to prey comes from reports of coccinelids that completely ingest relatively small aphids and switch to EOD when con­suming relatively large aphids (41, 44). While younger coccinelid larvae con­sistently used EOD for prey consumption, older larvae and adults frequently ingest entire prey. This observation again emphasizes the importance of EOD when the relative size ratio of predator to prey is low (44).

Scymnodes lividigaster (1) and several other relatively small coccinelids (44) were observed to bite into the aphid prey and begin to pump digestive juices and suck them back repeatedly. The digestive juices progressively liquify the prey's solid contents. The aphid body swells, apparently owing to turgor pressure (AC Cohen, unpublished observation). Many coccinelids, as well as dytiscids, have mandibles modified with canals for efficient delivery of diges­tive secretions (41, 44). These sickle-shaped mandibular structures exhibit remarkable parallels with the injection mechanisms of the neuropterans (13,

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

EXTRA-ORAL DIGESTION 99

6 2), including the muscular cibarial pump. Several other families of beetles are known to use EOD, including Haliplidae, Amphizoidae, Gyrinidae, Staphylinidae, Hydrophilidae, Phengodidae, Lampyridae, Cantharidae, and Cleridae (10, 29,48).

Diptera Larval Brachycera possess mandibles that are modified as piercing organs rather than biting or chewing structures (8, 9, 24, 67). Tabanid and rhagionid larvae have mandibles with canals that are regarded as poison ducts for delivery of venom and digestive secretions into the prey (95). An important modification of the feeding apparatus in predatory Brachycera is the loss in adults of the mandibles and their replacement by the hypopharynx as the principal feeding structure for injection of digestive secretions and the inges­tion of liquified food (67). This trend occurs in Empididae (8), Rhagionidae (8, 9, 56), and Asilidae (102). Adult asilid flies produce salivary digestive enzymes that include proteinases that are injected into prey where they digest the prey's contents (102). The asilid feeding apparatus is a highly evolved structure in which the mandibles and maxillae are essentially degenerate, and the hypopharynx is used both as a hypodermic needle for injection of salivary secretions and for uptake of liquified food (50, 6 7, 86 ). Details of the digestive chemistry of the predaceous asilids as well as those concerning other dipterous predators are unknown. Accounts of the feeding of asilids, larval syrphids, and other predaceous flies strongly implicate an important EOD component, but detailed and systematic diagnoses are lacking for this order.

CONCLUSIONS AND PER SPECTIVES

EOD is used by some or all members of 79% of predaceous terrestrial arthropod families. EOD, which evolved independently at least 24 times, is a means of ingesting concentrated nutrients from prey. Its ecological importance stems from its expansion of the predatory scope or the size range of prey that can be eaten. It also has a strong impact on handling time, partial consumption of prey, and optimal foraging strategies. It requires special modifications of behavior and morphology to deliver digestive enzymes to the prey's interior. Enzymes are either refluxed from the gut and reused repeatedly by refluxing predators, or they are injected and ingested with prey contents only once in nonrefluxing predators. Many facets of EOD remain to be clarified, including the considerable gaps in our knowledge of the biochemistry of enzymes and cofactors; the biomechanics and neurobiology of the enzyme-delivery systems; the morphology, especially the ultrastructure, of the feeding apparatus; and the behavioral ecology, including the relationship between partial consumption and physiology. Because EOD crosses so many phylogenetic lines and repre­sents such a confluence of different levels of biological organization, it stands

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

1O0 COHEN

as a fruitful subject of studies in comparative biology and cross-disciplinary approaches such as behavior and physiology, neurobiology and biomechanics, biochemistry and morphology, and ecology and evolution. Such interactive and comparative approaches to EOD should provide a deeper understanding of the nature of organisms that are keystone species in many terrestrial eco­systems.

ACKNOWLEDGMENTS

I thank Elizabeth Bernays, Tom Henneberry, Hollis Flint, John Law, John Edwards, Jacqueline Cohen, and Marilyn Reega for helpful comments on earlier versions of this manuscript.

Any Annual Review chapter, as well as any article cited in an Annual Review chapter, may be purchased from the Annual Reviews Preprints and Reprints service.

1-800-347-8007; 415-259-5017; email: arpr@class.org

Literature Cited

1. Anderson JME. 1981. Biology and dis­tribution of Scymnodes lividigaster (Mulsant) and Leptothea galbula (Mul­sant), Australian ladybirds (Coleoptera: Coccinellidae). Proc. Linn. Soc. N.S. W. 105:1-15

2. Backus EA. 1988. Sensory systems and behaviors which mediate hemipteran plant-feeding: a taxonomic overview. 1. Insect Physiol. 34: 151-65

3. Bailey PCE. 1986. The feeding behavior of a sit-and wait-predator, Rallatra dis­par (Heteroptera: Nepidae): optimal for­aging and feeding dynamics. Dec% gia 68:291-97

4. Baldwin E. 1967. Dynamic Aspects of Biochemistry. Cambridge, UK: Cam­bridge Univ. Press. 466 pp.

5. Baptist BA. 1941. The morphology and physiology of the salivary glands of Hemiptera-Heteroptera. Q. 1. Micro­scop. Sci. 83:91-139

6. Barnes RD. 1974. Invertebrate Zoology. Philadelphia: W.B. Saunders. 870 pp.

7. Bennet-Clark HC. 1963. Negative pres­sure produced in the pharyngeal pump of the blood-sucking bug, Rhodnius prolixus. 1. Exp. BioI. 40:223-29

8. Bletchley JD. 1954. The mouthparts of the dance fly, Empis livida L. (Diptera, Empididae). Proc. Zool. Soc. London 123: 143-65

9. Bletchley JD. 1955. The mouthparts of the Down-looker fly, Rhagio (= Leptis) scolopacea (L.) (Diptera, Rhagionidae). Proc. Zool. Soc. London 125:779-94

10. Borror OJ, Triplehorn CA, Johnson NF. 1989. An Introduction to the Study of Insects. Fort Worth, TX: Harcourt Brace College. 875 pp.

11. Bugnion E. 1929. Le ver-luisant pro­vencal et la luciole nicoise. Mem. Assoc. Nat. Nice Alpes-marit pp. 1-131

12. Burgess E. 1883. The structure of the mouth in the larva of Dytiscus. Proc. Boston Soc. Nat. Nist. 21:223-28

13. Buschinger A, Bongers A. 1969. Zur extraintestinalen Verdauung des Ameis­enlowen (Euraleon nostras Fourcr., Myrmeleontidae). Z. Vgl. Physioi. 62: 205-13

14. Chapman RF. 1969. The Insects Struc­ture and Functioll. New York: Elsevier. 819 pp.

15. Charnov EL. 1976. Optimal foraging, the marginal value theorem. Theor. Pop. BioI. 9:129-36

16. Cheeseman MT, Gillott C. 1987. Or­ganization of protein digestion in Calosoma calidum (Coleoptera: Carabi­dae). l. Insect Physiol. 33:1-18

17. Chippendale GM. 1978. The functions of carbohydrates in insect life processes. In The Biochemistry of Insects, ed. M Rockstein, pp. I-55. New York: Aca­demic. 649 pp.

18. Cobben RH. 1978. Evolutionary trends in Heteroptera. Part II. Mouthpart-struc­tures and feeding strategies. Meded. Lalldbouwhogesc/z. Wagenillgen. 78(5): 1-707

19. Cobben RH. 1979. On the original feed-

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

ing habits of the Hemiptera (Insecta): a reply to Merrill Sweet. Ann. Entomol. Soc. Am. 72:711-15

20. Cohen AC. 1984. Food consumption, food utilization and metabolic rates of Geocoris punctipes [Het.: Lygaeidae] fed Heliothis virescens [Lep.: Noctui­dae) eggs. Entomophaga 29 :361-67

21 . Cohen AC. 1989. Ingestion and food consumption efficiency in a predaceous hemipteran. Ann. Entomol. Soc. Am. 82: 495-99

22. Cohen AC. 1990. Feeding adaptations of some predatory hemiptera. Ann. En­tomol. Soc. Am. 83:1215-23

23. Cohen AC. 1993. Organization of di­gestion and preliminary characterization of salivary trypsin-like enzymes in a predaceous heteropteran, Zelus renardii. J. Insect Physiol. 39:823-29

24. Cook EF. 1949. The evolution of the head in the larvae of the Diptera. Mi­croentomology 14:1-57

25. Cook RM, Cockrell BJ. 1978. Predator ingestion rate and its bearing on feeding time and the theory of optimal diets. 1. Anim. Eco!. 47:529-47

26. Edwards JS. 1961. The action and com­position of the saliva of an assassin bug Platymeris rhadamantus Gaetst. (Hemi­ptera, Reduviidae). 1. Exp. Bioi. 38:61-77

27. Enders F. 1975. The influence of hunt­ing manner on prey size, particularly in spiders with long attack distances (Ara­neidae, Linyphiidae, and Salticidae). Am. Nat. 109:737-63

28. Ernsting G, Van Der Werf DC. 1988. Hunger, partial consumption of prey and prey size preference in a carabid beetle. Ecol. Entomol. 13:155-64

29. Evans G. 1975. The Life of Beetles. London: George Allen & Unwin. 232 pp.

30. Evans GO. 1992. Principles of Acarol­ogy. Oxon, UK: CAB Int. 563 pp.

31. Evans GO, Sheals JG, Macfarlane D. 1961. The Terrestrial Acari of the Brit· ish Isles, Vol. 1. London: British Mu­seum Nat. Hist. 219 pp.

32. Faucheux MMJ. 1975. Relations entre I' ultrastructure des sty lets et man­dibalaires et maxillaires et la prise de nourriture chez les Insectes Hemipteres. C. R. Acad. Sci. Ser. D 281:41-44

33. Foelix RF. 1982. Biology of Spiders. Cambridge, MA: Harvard Vniv. Press. 306 pp.

34. Gans C, Parsons TS, eds. 1969 . Biology of the Reptilia, Vols. 1-10. New York: GP Puntnam's Sons

35. Giller PS. 1980. The control of handling time and its effects on the foraging

EXTRA-ORAL DIGESTION 101

strategy of a heteropteran predator, No­toneeta. 1. Anim. Ecol. 49:699-712

36. Gilmour D. 1961. The Biochemistry of Insects. New York: Academic. 343 pp.

37. Goodchild AIP. 1966. Evolution of the alimentary canal in the Hemiptera. Bioi. Rev. 41:97-140

38. Griffiths D. 1980. Foraging costs and relative prey size. Am. Nat. 116:743-52

39. Griffiths D. 1982. Tests of alternative models of prey consumption by preda­tors, using ant-lion larvae. J. Anim. Ecol. 52:363-73

40. Habermehl O. 1975. Die biologische Bedeutung tierischer Gifte. Naturwis­senschaften 62:15

41. Hagen KS. 1986. Nutritional ecology of terrestrial insect predators. In Nutri­tional Ecology of Insects, Miles, Spiders and Related Invertebrates, ed. F Slan­sky, Jr, JG Rodriguez, pp. 533-77. New York: John Wiley & Sons

42. Hassell MP. 1978. The Dynamics of Arthropod Predator-Prey Systems. Princeton, NJ: Princeton Univ. Press. 237 pp.

43. Hespenheide HA. 1973. Ecological in­ferences from morphological data. Rev. Syst. Ecol. 4:213-99

44. Hodek I. 1973. Biology of Coecinelli­dae. Prague, Czechoslovakia: Junk, N.V. 260 pp.

45. Holling CS. 1964. The analysis of com­plex population processes. Can. Enlo­mo!' 96:335-47

46. Holling CS. 1966. The functional re­sponse of invertebrate predators to prey density. Mem. Emollloi. Soc. Can. 48:1-86

47. House HL. 1974. Digestion. In The Physiology of Insecta, ed. M Rockstein, 5:63-120. New York: Academic

48. Imms AD. 1947. In Insect Natural His­tory, pp. 123-78. Surrey, UK: Love & Malcomson

49. Jordan H. 1910. Uber extraintestinale Verdauung im allgemeinen und bei Carabus auratus im besonderen. Bioi. Zelltralbl. 30:85-96

50. Kahan D. 1964. The toxic effect of the bite and the proteolytic activity of the saliva and stomach contents of the rob­ber flies (Diptera, Asi1idae). IsraelI. Zool. 13:47-57

51. Kaiser E, Raab W. 1967. Collagenolytic activity of snake and spider venoms. Toxieon 4:251

52. Kaspari M. 1990. Prey preparation and the determinants of handling time. Anim. Behav. 40:118-26

53. Khan MA. 1964. Proteolytic activity in the digestive tract of the water scorpion

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

102 COHEN

Laccotrephus maculatus. Entomol. Exp. Appl. 7:335-38

54. Kingsolver 10, Daniel TL. 1993. Me­chanics of fluid feeding in insects. In Functional Morphology of Insect Feed­ing, Proc. Thomas Say Publications in Entomology, ed. CW Schaefer, RAB Leschem, pp. 149�1. Lanham, MD: Entomo!. Soc. Am.

55. Koch M, Bongers J. 1981. Nahrung­serwerb des Ameisenlowen Euroleon nostras Fourcr. Neth. l. Zool. 31 :713-28

56. Krystoph H. 1961. Vergleichend-mor­phologische Untersuchungen an den Mundteilen bei Empididen. Beitr. Ento­mol. 11:824-72

57. Lavoipierre MM, Dickerson JG, Gordon RM. 1959. Studies on the methods of feeding of blood-sucking arthropods. Ann. Trop. Med. Parasitol. 53:235-50

58. Law lH, Dunn PE, Kramer KJ. 1977. Insect proteases and peptidases. Adv. Ellzymol. 45:389-425

59. Legendre R. 1978. Quelques progres recents concernant I'anatomie des araignees (systeme nerveux sympa­thique et appareil digestit). In Arach-1I010gy, Sevellth Illternatiollal COllgress Symposium of the Zoological Society of Lolldoll, ed. P Merret, 42:379-88. Lon­don: Academic

60. Lengerken H. 1 924. Extraintestinale Verdauung. Bioi. Zelltralbl. 44:273-95

61. Lewis JGE. 1982. The Biology of Cell­tipedes. Cambridge, UK: Cambridge Univ. Press. 476 pp.

62. Lozinski P. 1908. Beitrag wr Anatomie und Histologie der Mundwerkzeuge der Myrmeleonidenlarven. Zool. Anz. 33: 473-84

63. Lucas JR. 1985. Partial prey consump­tion by ant-lion larvae. Anim. Bellav. 33:945-58

64. Lucas JR, Grafen A. 1985. Partial prey consumption by ambush predators. l. Theor. Bioi. 113:455-73

65. Manton SM. 1965. The evolution of arthropod locomotory mechanisms. Part 8. Functional requirements and body design in Chilopoda, together with a comparative account of their skele­tomuscular systems and an appendix on the comparison between burrowing forces of annelids and chilopods and its bearing upon the evolution of the arthropodan haemocoel. J. Lillll. Soc. Zool. 46:251-483

66. Manton SM. 1973. Arthropod phylo­geny-a modern synthesis. l. Zool. LOII­don 1 7l : 1 l l-30

67. Matsuda R. 1965. Morphology and evo­lution of the insect head. Mem. Am. Elltolllol. fllst. Anll Arbor pp. 1-334

68. McCormick SJ, Polis GA. 1990. Prey, predators and parasites of scorpions. In The Biology of Scorpions, ed. GA Polis. Stanford, CA: Stanford Univ. Press . 587 pp.

69. McCrone JD, Hatla RI. 1967. Isolation and characterization of a lethal com­pound from the venom of Latrodectus mactans mactans. In Animal Toxins, ed. FE Russel, PR Saunders, p. 29. New York: Pergamon

70. Miles PW. 1972. The saliva of Hemip­tera. Adv. Illsect Physiol. 9: 188-256

7 1 . Millot J. 1931. Anatomie comparee de l 'intestin moyen cephalothoracique chez les araignees vraies. C. R. Acad. Sci. Paris 192:375-77

72. Millot 1. 1931. Les diverticules in­testinaux du cephalothorax chez les araignees vraies. Z. Morph. Okol. Tiere 21:74�

73. Millot J. 1926. Contribution a l'histo­phyiiologie des areneides. Bull. Bioi. Franc. Belg. Supp!. 8:1-28

74. Metzenauer P 1981 . Extraintestinale Verdauung bei Carabus problematicus Herbst im Vergleich mit Pterostichus nigrita (Paykull) (Col., Carabidae). Zool. Anz. lena 206:57�1

75. Metzenauer P, Kloft VJ. 1981 . Nahrung­spassage bei dem carnivoren Laufkafer Pterostichus (Pseudomaseus) nigrita (Paykull) (Col., Carabidae). Zool. Anz. 206:154-60

76. Mittler TE. 1967. Flow relationships for hemipterous sty lets. Ann. Entomol. Soc. Am. 60: l l 12-14

77. Mommsen TP. 1978. Digestive enzymes of a spider (Tegenaria atrica Koch). 1. General remarks, digestion of proteins. Compo Biochem. Physiol. 60A:371-75

78. Mommsen TP. 1978. Digestive enzymes of a spider (Tegenaria atrica Koch). II. Carbohydrases. Compo Biochem. Physi-01. 60A:371-75

79. Mommsen TP. 1978. Digestive enzymes of a spider (Tegellaria atrica Koch). III. Esterases, phosphatases, nucleases. Compo Biochem. Physiol. 60A:377-82

80. Mommsen TP. 1978. Comparison of digestive a-amylases from two species of spiders (Tegenaria atrica and Cupi­ellllius solei). l. Compo Physiol. 127B: 355-61

8 1 . Mommsen TP. 1980. Chitinase and �­N-acetylglucosaminidase from the di­gestive fluid of the spider, Cupiennius salei. Biochim. Biophys. Acta 612:361-72

82. Nagel W A. 1890. Uber eiweissver­dauenden Speichel bei Insekten-Larven. Bioi. Zelltralbl. 16:51

83. Nentwig W. 1989. Seasonal and taxo-

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.

nomic aspects of the size of arthropods in the tropics and its possible influence on size-selectivity in the prey of a tropi­cal spider community. Oec% gia 78: 35-40

84. Nentwig W, Wissel C. 1986. A com­parison of prey lengths among spiders. Oecologica 68:595-600

85. O'Brien JW, Evans BI, Howard lB. 1 989. Flexible search tactics and effi­cient foraging in saltatory searching ani­mals. Oecologia 80:100-10

86. Oldroyd H. 1960. The Natural History of Flies. London: Weidenfeld and Ni­colson. 324 pp.

87. Plateau F. 1877. Recherches sur la struc­ture de I' appareil digestif et sur les phenomenes de la digestion chez les araneides dipneumones. Bull. Acad. R. Be/g. 44:129-45

88. Pollard SD. 1988. Partial consumption of prey: the significance of prey water loss on estimates of biomass intake. Oecologia 76:475-76

89. Pollard SD. 1993. Little murders. Nat. Hist. 1 02:58-65

90. Prosser CL. 1973. Comparative Animal Physiology. Philadelphia: W. B. Saun­ders. 966 pp.

91. Rastogi Sc. 1962. On the salivary en­zymes of some phytophagous and pre­daceous heteropterans. Sci. Cult. 28:479-80

92. Rees AR, Offord RE. 1969. Studies on the protease and other enzymes from the venom of Let/wcerus cordofanus. Nature 221:665-67

93. Savory T. 1977. Arachnida. London: Academic. 340 pp.

94. Schmidt JO. 1982. Biochemistry of in­sect venoms. AIII!1I. Rev. Elltomoi. 27: 239-68

95. Schremmer F. 195 1 . Die Mundteile der Brachycerenlarven und der Kopfbau der Larve von Stratiomys chamaeieon L. Osterr. Zoot. Zeits. 3:326--97

96. Sih A. 1 980. Optimal foraging: partial consumption of prey. Am. Nat. 1 1 6:281-90

EXTRA-ORAL DIGESTION 103

97. Smith JJB. 1985. Feeding mechanisms. In Comprehensive Insect Biochemistry, Physiology and Pharmacology, ed. GA Kerkut, LI Gilbert, 4:33-85. Oxford: Pergamon

98. Snodgrass RE. 1935. Principles of In­sect Morphology. New York: McGraw­Hill. 667 pp.

99. Sweet MH. 1979. On the original feed­ing habits of Hemiptera (Insect). Ann. Entomol. Soc. Am. 72:575-79

99a. Vonk HI, Western IRH. 1984. Com­parative Biochemistry and Physiology of Enzymatic Digestion. London: Aca­demic. 501 pp.

100. Weber H. 1928. Ske1ett, Muskulatur und Darm der schwarzen Blattlaus, Aphis fabae Scop. Zoologica StlIttgart 28:1-120

101. Weber H. 1928. Zur vergleichenden Physiologie der Saurgorgane der Hemipteren mit besonderer Berilck­sichtigung der PflanzenHiuse. Z. Vgl. Physiol. 8: 1 45-86

102. Whitfield FGS. 1925. The relation be­tween the feeding habits and the struc­tures of the mouthparts in the Asilidae (Diptera). Proc. Zool. Soc. London pp. 599-638

103. Wigglesworth VB. 1972. The Principles of Insect Physiology. London: Chapman and Hall. 827 pp.

1 04. Wilson EO. 1992. The Diversity of Life. New York: W.W. Norton. 423 pp.

105. Woodring JP, Carter SC. 1 962. The internal anatomy. reproductive physiol­ogy, and moulting process of Cera­tozetes eisalpinus (Acarina: Oribatei). All/!. Elltolllol. Soc. Am. 55:164--81

106. Wundt H. 196 1 . Der Kopf der Larvae OSlIlyillS chrysops L. (Neuroptera, Planipennia). Zool. lahrb. Abt. Anat. 011 tog. Tiere 79:558-662

107. Deleted in proof 108. Zimmermann EW. 1934. Untersuchun­

gen uber den Bau des Mundhohlen­daches der Gewebespinnen. Rev. Suisse Zool. 41 :149

Ann

u. R

ev. E

ntom

ol. 1

995.

40:8

5-10

3. D

ownl

oade

d fr

om w

ww

.ann

ualr

evie

ws.

org

by U

nive

rsity

of

Haw

aii a

t Man

oa L

ibra

ry o

n 09

/10/

13. F

or p

erso

nal u

se o

nly.