Arthropod Biology:
Revision Notes

Compiled as a final-year zoology student at the University of Edinburgh, based on the information given in lectures.

Characteristics of the phylum Arthropoda

Open circulatory system - main body cavity is a haemocoel.
Body segmented, with specialisation of particular segments (tagmatisation), and jointed appendages.
Well developed chitinous exoskeleton, with growth by moulting (ecdysis).
Head usually bears a pair of lateral compound eyes and one to several simple median eyes.
Nervous system with dorsal brain (cerebral ganglia) and paired ventral nerve cords with ganglion in each segment.
Functional cilia absent (except for sperm of a few groups).

Major groups of arthropods

Trilobitamorpha - trilobites and their relatives (extinct).

Crustacea - 5-segmented head and long body; generally have cephalic shield or carapace; appendages primitively biramous; lifecycle usually involves a nauplius larva. Includes (amongst other groups):

Maxillopoda - ostracods, copepods, barnacles, etc.
Malacostraca - decapods (e.g. crabs), krill, isopods (e.g. woodlice), amphipods (e.g. Gammarus), etc

Chelicerata - body composed of anterior prosoma (cephalothorax) and posterior opisthosoma (abdomen), prosoma bears chelicerae, pedipalps and 4 pairs of uniramous walking legs; suctorial feeders (no jaws); breathe with book lungs, book gills or tracheal tubes. Consists of:

Merostomata - extinct sea scorpions (eurypterids), horseshoe crabs
Arachnida - spiders (Araneae), harvestmen (Opiliones), scorpions, pseudoscorpions, ticks and mites (Acari), etc

Pycnogonida - sea spiders - weird and poorly known, related to chelicerates

Myriapoda - body is a line of more-or-less similar trunk segments, lacking clear tagmatisation. Consists of:

Progoneata - millipedes (Diplopoda etc) - herbivorous
Chilopoda - centipedes - carnivorous

Hexapoda - insects and their relatives. Consists of:

Apterygota (Ametabola) - primitively wingless. Includes: bristletails, silverfish, etc.
Exopterygota (Hemimetabola) - wings develop externally, no pupal stage in life cycle. Includes: palaeopteran types with no wing-folding ability (mayflies, dragonflies), orthopterid types with mandibles (stoneflies, cockroaches, termites, stick insects, earwigs, etc), and hemipteroid types with sucking mouthparts (bugs, lice, etc).
Endopterygota (Holometabola) - wings develop internally, full metamorphosis. Includes: scorpion flies, lacewings, butterflies (Lepidoptera), caddis flies, true flies (Diptera), fleas, bees/ants/wasps (Hymenoptera), beetles (Coleoptera), etc.

Patterns in arthropod diversity

Some groups have survived, while others have perished. Were trilobites a poor design? No.
Variation in diversity of form. Why do crustaceans and chelicerates show more morphological diversity than insects? They are more ancient? They have more limbs and segments to modify? (But also true of myriapods, which aren't diverse.) They inhabit a wider range of niches?
Variation in biomass. Why is there such a high crustacean biomass? Habitat productivity, habitat availability (oceans are vast and three-dimensional), habitat diversity (crustaceans can survive in temporary pools etc).
Variation in species richness. Why are insects and mites more species rich than crustaceans? Greater variety of habitats on land than in water. Adaptation to specific hosts (Fahrenholz's Rule - host diversity drives parasite diversity) - terrestrial plants are structurally complex, and eating them may also require specific detoxification mechanisms. Additional reasons for insect diversity: more localised niches (no planktonic larval dispersal), ability to locate dispersed habitat patches (flight), ability to cope with concealed resources (underground, inside other organisms), holometabolous life cycles (allow adults and larvae to exploit different niches).
Variation in range of habitats occupied. Why are there hardly any marine insects? Insects can cope with salt lakes etc on land. Insect adaptations (e.g. wings) are inappropriate in the sea? Hard to prove. Crustaceans already occupy marine niches?

Hormones, moulting and metamorphosis

(Nijhout 1994, Insect hormones)

Ecdysones, steroid hormones secreted by the prothoracic gland, drive the moulting cycle. Ecdysone release is triggered by release of PTTH from corpus cardiacum of brain (release is under neural control).
Metamorphosis appears to have evolved once - Holometabola are monophyletic (Truman & Riddiford 1999).
Juvenile Hormone (JH) is secreted by corpus allatum of brain. Absence of JH during a sensitive period leads to metamorphosis. Artificial injection of JH can keep insects in larval state.
There is a delay between achievement of critical weight and pupation, due to time taken for JH to be cleared. JH inhibits action of PTTH during final larval instar.
Photoperiodic gates may be associated with hormone release, so it can only occur at certain times of day.
Moult cycle is tied to growth - insects can be artificially kept in larval stages by restricting food intake.
In the hemipteran bug Oncopeltus, moulting occurs when a critical weight is reached (Nijhout 1971).
Restricted feeding experiments on the moth Manduca - if size is below critical threshold at end of 'final' larval instar, extra instars result (Nijhout 1975). Contrast with Drosophila, where there are always three larval instars.
In Hemiptera, abdominal stretch provides a measure of growth - artificially inflating bugs triggers moulting. In Lepidoptera and Diptera, nutrient levels appear to be the cue.
Many insects undergo diapause in response to short day length, although exact mechanism varies between species.
In Manduca, brains removed from larvae, exposed to long photoperiods in vitro, and implanted into short-day larvae 'reprogram' them into long-day larvae (Bowen et al 1984).
In the blowfly, Calliphora, diapause in larvae depends upon photoperiod experienced by the mother. Critical day length is higher in populations from more northerly latitudes (McWatters & Saunders 1996).

Polyphenism

The ability to develop in different ways depending upon the conditions experienced during development...

Seasonal diphenism in butterflies - in Araschnia levana, short-day larvae diapause and emerge as red spring morphs, long-day larvae don't diapause and emerge as black & white summer morphs. Experiments involving parabiosis and ecdysone injection show that timing of ecdysone release determines which morph develops. In other butterflies (e.g. Polygonia), seasonal diphenism is controlled by a brain-borne 'summer morph producing hormone' rather than by timing of ecdysone release (Koch & Buchmann 1987). The butterfly Precis coenia has beige long-day morph (linea) in spring/summer and reddish-brown short-day morph (rosa) in autumn; temperature as well as photoperiod determines which morph develops (Rountree & Nijhout 1995).
Horn polyphenism in dung beetle Onthophagus taurus - larger males have disproportionately large horns (for fighting), small males have tiny, useless horns. Metamorphosis occurs when food runs out; body size at metamorphosis determines whether large- or small-horned form develops. Horn development triggered by JH at a critical period - demonstrated by artificially applying methoprene, a JH analogue (Emlen & Nijhout 1999).
Soldier determination in ant Pheidole bicarinata – development as a soldier depends on JH and on a critical body size. Addition of methoprene to larger larvae causes them to develop into soldiers; addition of methoprene to smaller larvae does not (Wheeler & Nijhout 1983). Nursing of larvae by soldiers, rather than by workers, inhibits them from becoming soldiers themselves, apparently by a pheromonal mechanism (Wheeler & Nijhout 1984).

The cuticle

Functions of exoskeleton: acts as a template for body form, facilitates levers for locomotion, allows development of hard structures such as jaws, and reduces water loss.
Annelids are segmented like arthropods (though not closely related), and can make sclerotised appendages (e.g. jaws), but their bodies never became entirely hardened due to limitations of hydrostatic skeleton.
Dyar's law - amount of growth at each moult is predictable: instar number is proportional to log(body dimension).
Przibram's law - at each instar weight doubles and dimensions increase by 1.26 times (assuming isometric growth).
Exoskeleton is like a strong tube. Increasing diameter increases strength, but also weight, limiting arthropod size.
Layers of cuticle: basement membrane (with epidermal cells), procuticle, and epicuticle.
Procuticle is made of criss-crossed strands of chitin (a polysaccharide), with high flexibility and tensile strength, and protein (arthropodin), tanned to form sclerotin. Tanning occurs from outside in, resulting in hard exocuticle and plastic endocuticle. At hinges in exoskeleton, exocuticle is absent and resilin (elastic protein) gives flexibility.
Epicuticle comprises inner and outer layers of cuticulin (protein/lipid mixture) covered by waterproof wax layer (secreted by epidermal cells through pore canals) and cement layer (secreted by extensions of dermal glands).
Stages of moulting: apolysis (splitting of epidermis from base of old cuticle), ecdysis (shedding of cuticle).
Inactive moulting fluid fills gap between old and new cuticle while epidermis lays down cuticulin layer of new cuticle; fluid is then activated and digests old endocuticle. Insect expands by swallowing air or water (haemocoel may have evolved to facilitate this); old exocuticle and epicuticle rupture along ecdysial lines (where exocuticle is thin) and are shed. New cuticle is sealed, waterproofed, and finally sclerotised.
Ecdysis is triggered by eclosion hormone (EH). Sclerotisation of cuticle is also driven by hormones (bursicon).
Cuticle waxes lose much of their waterproofing ability when a certain temperature is exceeded.
Outer ends of gut and tracheal tubes are also lined by cuticle and must be shed during moulting.

Nutrition, growth and body size

(Nijhout 2003, Stern 2003)

Metamorphosis in Manduca is triggered by drop in JH levels when critical body size is reached. Lab populations of Manduca kept since 1970s have increased in size, due to greater growth in final larval instar (higher critical weight, longer time taken to clear JH, and higher growth rate). Why? Inadvertent selection by lab technicians for body size? Release from constraints imposed by natural selection?
Some insects (e.g. Drosophila) won't pupate at all if they fail to reach a critical body size; others (e.g. Manduca) will eventually metamorphose into undersized adults if persistently underfed.
Artificial selection can increase body size in Drosophila, with increased critical weight and increased delay between achievement of critical weight and metamorphosis. Increase is in cell number rather than cell size.
Control of imaginal disc growth in Drosophila is largely intrinsic to the disc - it grows to a predefined size. There is also extrinsic control by insulin-like proteins, whose production depends on nutrient levels (Ikeya et al 2002).
There is feedback from the growing imaginal disc to the rest of the body - delaying disc growth (by removing parts and forcing regeneration) will delay pupation of the whole insect.
Growth of lepidopteran imaginal discs in vitro requires the insulin-like protein bombyxin (Nijhout & Grunert 2002).
Drosophila, like many ectothermic animals, grows more slowly but ultimately larger at low temperatures. Natural selection under cold temperatures produces cool lines that develop faster and larger at normal temperatures. Experiments suggest these differences are adaptive (cold types are fitter under cold conditions and vice versa).
Latitudinal clines in size of Drosophila are found in Australia and South America. In Australia (where spread may have been from north to south so selection was for increased size) the difference is mostly in cell number; in South America (where selection may have been in both directions) it is in both cell size and number.
Size evolution may reflect trade-offs - restricted feeding experiments show that growth is more efficient at lower temperatures, so low-temperature populations incur fewer costs in growing larger (Robinson & Partridge 2001).

Butterfly wing patterns

Seasonal polyphenism - in Pontia occidentalis, spring morph darker than summer morph; experiments (correlation between melanism and survival, rearing butterflies with wrong photoperiods, painting butterflies) suggest this is related to thermoregulation (Kingsolver 1995). In Bicyclus anynana, wet season morph with prominent eye spots develops in warm conditions; camouflaged dry season morph develops in cooler conditions (Brakefield 1996).
Eye spot colour develops in response to signal emitted from centre (focus) - grafting experiments demonstrate this (McMillan et al 2002).
Artificial selection can produce variation in eye spots. There is a correlated response between different eye spots, although this correlation can be broken by deliberate selection.
Muuml;llerian mimicry in Heliconius - H. erato and H. melpomene have different morphs in different regions of South America. Local morphs of the two species mimic one another. Capture-release experiments show that this mimicry is linked to survival. Colour patterns are due to 20 tightly-linked genetic loci. Where H. melpomene coexists with closely-related H. cydno, its mating preferences are stronger - selection against hybridisation (Jiggins et al 2001).
Polymorphism in Heliconius either arose historically when habitat was split into refugia, or results from one species adapting to local environments and the other arriving later and mimicking it. Phylogenies of H. erato and H. melpomene are different, and colour morphs do not correspond to genetically distinct races, suggesting the latter hypothesis. Divergence in H. melpomene is more recent, so maybe it was the newcomer. (Brower 1996)

Compound eyes

Insect compound eyes are rhabdomeric, consisting of many ommatidia.
Photoreceptor cells have many microvilli, carrying visual pigment molecules.
Visual pigment consists of a chromophore (a Vitamin A aldehyde derivative) bonded to a protein (opsin). Photon capture alters the isomeric status of the chromophore molecule from an 11-cis (bent) conformation to an all-trans (straightened) form, starting a cascade of reactions leading to perception of vision.
Types of compound eye: Apposition eyes, with photoreceptors directly under the lenses, allow the formation of an (inverted) image. Superposition eyes, with photoreceptors at the bottom of the ommatidia (separated from the lenses), are good in low-light conditions and are used by night-flying insects. Neural superposition eyes, containing optically-isolated ommatidia in which photoreceptors all point in the same direction, allow the formation of complex images, and are found in dipterans.
Some arthropods also have simple eyes (ocelli).
Insect eyes have hexagonal lenses, because this shape packs together most efficiently. Crustacean eyes are composed of square units, each side of which is a shiny mirror (mirrors work better than lenses underwater).
Each ommatidium of a dipteran eye has a set of 8 photoreceptors, which are sensitive to different wavelengths, allowing perception of different colours (including UV).
Visual pigment is bistable, with visually-active xanthopsin (similar to rhodopsin in vertebrate eyes) present under dark-adapted conditions, and inactive metaxanthopsin predominating under light-adapted conditions.
Transition from active to inactive pigment is triggered by blue light; reactivation of pigment is triggered by red light (Wright & Cosens 1977). This process is much faster than the reactivation of pigment in vertebrate eyes (which is enzyme-catalysed), allowing insects to cope with a rapidly-changing visual-environment (e.g. when flying through a forest), and permitting a high flicker-fusion rate (which requires a high level of active visual pigment). Red pigment in eyes encourages reactivation of visual pigment molecules.
Maximum absorption of light occurs when plane of polarisation is parallel to long axis of pigment molecule.
In insect eyes pigment molecules are parallel to long axis of microvilli, permitting sensitivity to polarisation.
In bees' ommatidia, eight retinular cells are twisted 180° along their length (so have no overall polarity-detection ability), but a ninth is not (Wehner et al 1977). However, this turns out not to be the polarisation detector.
In bees and Cataglyphis ants, polarisation is detected in the dorsal rim area of the eye, where there is a two-channel system - some (UV-sensitive) cells respond most strongly to light with a particular plane of polarisation, and others to light with a different plane (Labhart 1980).

Endothermy and temperature regulation

(Heinrich 1993, The hot blooded insects)

Homeothermy (constant body temperature) and poikilothermy (body temperature varying with environment) are states. Endothermy (generating heat internally) and ectothermy (relying on external heat sources) are ways of achieving those states.
Mammals and birds maintain a constant temperature (36-40°C) by catabolism in the liver and in brown adipose tissue. Smaller mammals and birds lose heat faster; they compensate by having higher proportion of brown adipose tissue, elevated metabolic rate, and periods of torpor in which they thermoregulate at a lower temperature.
Endothermic vertebrates have a minimum size of around 2g. Large insects are capable of thermoregulation despite being much smaller than this.
Endothermy in insects allows high-performance activities (flight, singing in katydids and cicadas, dung-rolling in competitive dung beetles) to be conducted over a range of environmental temperatures. When not performing these activities, insects do not thermoregulate, yet are not totally inactive, unlike torpid mammals or birds.
For flight, insects maintain a high temperature only within the thorax. The thorax is relatively spherical and well-insulated (with scales, hairs, or air sacs at front of abdomen) to minimise heat loss.
Insects warm up by vibrating their powerful flight muscles while the muscles are disconnected from the wings. They may also generate heat by performing futile enzyme cycles, but this is uncertain. Time and cost of warm-up depend on the ambient temperature; below a minimum temperature, warm-up will not be attempted.
In bees, a counter-current heat exchanger at the petiole (waist) keeps warmth in the thorax when necessary.
Insects cool down by pulsing haemolymph between thorax and abdomen, transferring heat to the abdomen where it is lost through an uninsulated 'thermal window'. Bees can also cool down by 'tongue-lashing' (regurgitating nectar onto tongue where it evaporates).
Other uses of body heat by bees: incubation of larvae, maintenance of colony temperature, killing hornets - bees surround an invading hornet and heat it to a temperature that kills the hornet but not the bees (Ono et al 1995).
Endothermic ability varies between bee species, and within species (e.g. Amegilla sapiens, found at different altitudes in New Guinea), depending on climate.
Female bees, which must fly regularly to stock cells with food for young, are usually more endothermic than males (exception: the carder bee Anthidium, in which males guard flowers territorially and are highly endothermic).
Parasitic bees that deposit larvae in other bee species' nests are less endothermic than their hosts.

The origin of arthropods

Arthropods were traditionally thought to be related to annelids, which are also segmented and have paired segmental appendages. However, there are differences: annelids do not moult; annelids have ciliated trochophore larvae while crustaceans have nauplius larvae, most annelids have a coelom while arthropods have a haemocoel.
DNA sequence data has now led to arthropods being grouped with nematodes and related phyla (which also possess a haemocoel and chitinous cuticle, and moult) into the Ecdysozoa (Aguinaldo et al 1997). They are not closely related to annelids, which evolved segmentation independently.
Lobopods (onychophorans and tardigrades) are the arthropods' closest living relatives. Arthropods probably evolved from a lobopod-like ancestor.
The trilobites, chelicerates, crustaceans and onychophorans are all ancient, dating back to Cambrian times.
Manton (1977) wrongly grouped insects, myriapods and onychophorans - which share uniramous limbs - together as the Uniramia. Manton believed that the Uniramia have jaws derived from whole-limbs while other arthropods have gnathobasic jaws (derived from a basal limb part). More recent evidence, from expression patterns of distal-less gene, suggests that all arthropods have gnathobasic jaws (Popadić et al 1998).
Molecular data shows that the arthropods are monophyletic, and that insects are most closely related to crustaceans (they are grouped together as the Pancrustacea). Very recent evidence (Nardi et al 2003) suggests that the Hexapoda are polyphyletic.
Some group Pancrustacea with myriapods as 'mandibulates' (Giribet et al 2001); others disagree (Hwang et al 2001).
Millipedes, centipedes, arachnids, crustaceans and the ancestors of insects all invaded the land independently.
The tracheae and malpighian tubules of insects and myriapods are convergent adaptations to life on land.

More notes and essays

Arthropod Biology: Revision Notes