Chrysis ignita

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Chrysis ignita
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Scientific classification OOjs UI icon edit-ltr.svg
Domain: Eukaryota
Kingdom: Animalia
Phylum: Arthropoda
Class: Insecta
Order: Hymenoptera
Family: Chrysididae
Genus: Chrysis
Species:
C. ignita
Binomial name
Chrysis ignita

Chrysis ignita is a species of cuckoo wasp. It is one of a group of species which are difficult to separate and which may be referred to as ruby-tailed wasps.

Contents

Cuckoo wasps are parasitoids and kleptoparasites, laying their eggs in the nests of other species where their young consume the larvae of their hosts. They have a number of adaptations which have evolved to equip them for their life cycle. They have metallic, armored bodies, and can roll up into balls to protect themselves from harm when infiltrating the nests of their hosts. Unlike most other aculeates, however, cuckoo wasps cannot sting.

The hosts of Chrysis ignita are believed to be potter wasps such as Ancistrocerus parietum . [1] [2] [3] Chrysis ignita is found across the Palearctic excluding Africa, from western Europe to China and Japan. [4]

Taxonomy and phylogeny

Chrysis ignita is a chrysidid wasp with a typical colorful, metallic exoskeleton; the stinger is reduced in size and used as an ovipositor. [5] [6]

Description and identification

Chrysidids differ from other aculeate wasps (stinging Hymenoptera) in their reduction of the number of external body segments, the presence of 11 antennal articles, and wing veins enclosing 5 cells. Chrysis ignita is the best known of a group of very similar ruby-tailed wasps. [7] The head and thorax range from a shiny green to blue, sometimes layered with a golden sheen. The abdomen, a deep ruby color, is its most distinctive feature. The exoskeleton sculpture appears textured, like a golf ball, with dimples, projections, crests, and holes ranging from micrometric to millimetric in size. [5]

Distribution and habitat

Chrysis ignita can be found in Britain and Ireland, in continental Europe, and through Russia to China and Japan at the eastern edge of the Palearctic. [1] [4] [8] [9] Its habitats overlap with those of its hosts, and thus it can be found near walls, quarries, bare cliff faces, and around dead wood in sunny places. [10] Since chrysidids are solitary wasps whose lives are linked to and dependent on their hosts, they live in strict microhabitats. These microhabitats can be further categorized as places of rest and of parasitic activity. The environments in which they are found facilitate their identification and are often characterized by flowers, arid and sandy soil, old wood exposed to sunlight, pebbles, and aphid infested plants. [5]

Life history

Infiltration and egg deposition

Chrysidids are parasitoids, meaning that their parasitic activity, in most cases, kills their hosts. Some species are also kleptoparasites, meaning that they also use the host's food supplies as resources to sustain themselves. Chrysis ignita is both a parasite and a kleptoparasite. The female wasp possesses a long, telescopic ovipositor, which evolved from the reduction of the aculeate stinging apparatus. She uses this appendage to deposit her eggs inside the nest of the host wasp. The female ruby-tailed wasp will hide nearby, waiting for an ideal host. She will look for wasps that are in the process of digging burrows or dragging prey or bringing food back to their nests. She will then observe the nest until the host leaves or hitch a ride on the prey to slip in. [5]

Parasitism

There are two basic strategies for parasitizing the host. In the first strategy, the cuckoo wasp eats the host egg or host young larva as soon as it hatches and moves on to eating the food resources in the nest (kleptoparasitism). In the second strategy, the cuckoo wasp waits for the host larva to reach its prepupal stage, and it kills it after clearing the nest of food sources. [11] Each strategy has its advantages. The second strategy is generally utilized when the host species is a nectar and pollen gatherer, stocking up its nests with food sources that contain nutrients the cuckoo wasp cannot synthesize itself. [5] If the host wasp is able to accumulate enough food to sustain both her offspring and the cuckoo larva, the cuckoo larva may consume only that food, leaving the host larva.

Morphology

In addition to bold coloration, cuckoo wasps tend to have large, bulging, well developed eyes. The head is generally flat or shallowly convex on the backside, without distinct bumps or grooves. In all cuckoo wasps, the occipital suture, or the groove at the back of the wasp's head, is reduced compared to in other wasp families. The majority of the lateral faces of the head are taken up by large compound eyes. See the insect anatomy category for vocabulary.

Face

Chrysidid faces, or the front of the head, distinguish them from other Hymenopterans. The antennae are attached low on the face, on the dorsal margin of clypeus. [9] Generally, the clypeus is short and broad, truncating at the apex. The dorsal margin extends around and partly enclose the antennal sockets. Chrysidids have simple mandibles, with usually one or two subapical teeth.

Abdomen

The number of visible chrysidid segments varies among subfamilies. Chrysis ignita has three segmented abdomens in both sexes, which make sex determination difficult. The morphology of the abdominal anatomy translates into defensive function for the wasp. The visible segments are heavily sclerotized and weakly intermusculated. [9] The abdominal segments I through IV possess spiracles, which the wasp breathes through. The chrysidid stinger is essentially nonfunctional, having been reduced to an ovipositor in females and a genital tube in males.

Coloration

Chrysis ignita is generally colored, and takes on its metallic, iridescent sheen through light interference, and thus varies with the viewing angle. The coloration is most apparent on the body of the wasp, and reduced to spots and stripes on the legs, mandibles, antenna, and abdominal tergites. [9] Identification of Chrysis species based on color can be difficult due to the ephemeral nature of their coloration. Chemicals used to kill, preserve, or rehydrate specimens can alter the wasp's colors. [9] It has also been hypothesized that there may be an environmental relation between the color of the adult and the physical parameters of its developmental environment, like temperature and humidity. [5]

Functional adaptions

Body armor and strategies

Chrysis ignita and its family of chrysidid wasps have evolved effective defenses for their risky life cycle. While the life of a cuckoo wasp may seem easy, it must drop off its young to be raised by a host wasp species. The ruby-tailed wasp has to infiltrate a nest full of defensive mother wasps, often armed with powerful stingers and jaws. Thus, they have developed defensive, functional body armor to protect themselves. The abdominal segments of their exoskeleton are highly sclerotized on the external surface and concave on the ventral surface. [5] This allows the wasp to tuck in its vulnerable antenna and legs when curling into a defensive sphere. This adaption prevents the ruby-tailed wasp from being stung or mutilated when sneaking around a potential host's nest. The defense is so effective that even when the mother is caught in the host's nest, she will simply ball up and become impenetrable to even the strongest stings and mandibles. [5] If they are caught, which happens quite often, they simply tuck and curl. The host wasp has no choice but to grab the balled up ruby-tailed wasp in its jaws and carry it outside to evict it. [12] The ruby-tailed wasp, unharmed, simply makes its way back into the nest again at the next opportunity.

Ovipositor

The ruby-tailed wasp possesses an ovipositor, which evolved from the usual stinging apparatus of most Hymenopterans. Ruby-tailed wasps have been reported to parasitize a variety of hosts, and thus their ovipositor has evolved to be a multi-tool for infiltrating the nests of different wasps. For example, in parasitizing the mud nest of a digger wasp, the female ruby-tailed wasp will first wet a point of the dry mud before attempting to saw through it with her ovipositor. [12] After several repetitions, she will succeed, and can then deposit her egg near or in the host wasp larval cell or cocoon. In the case of parasitizing paper wasp or mason bee, the ruby-tailed wasp's strong, indented ovipositor is used in a similar fashion to cut through the nest substrate to get to the host young. After the egg is deposited, the ruby-tailed wasp will cover the hole with the original nest material to leave minimal traces of its infiltration. It is essential that both she and her egg remain undetected to ensure the success of her offspring.

Known hosts

The hosts of Chrysis ignita sensu stricto are believed to be potter wasps such as Ancistrocerus parietum . [1] [2] [3] Chrysis ignita has been alleged to parasitize a wide variety of wasps and bees. [13] However, most of these host records, including all those of bee species, are considered doubtful: attributable to misunderstandings, misidentifications, and taxonomic inconsistency. [1] [3] [14]

Methods of field study

As with other species, study may proceed using a Malaise trap, the more basic Moericke trap, or simply hunting on sight. Alternatively, nests of host wasps can be bred in the hope that some will be parasitized by Chrysis ignita. [5]

Research interest

Accessory nuclei

Accessory nuclei (AN) are organelles of mysterious function found in oocytes. Oocytes are highly specialized cells, which not only contain cellular and molecular components that allow for fertilization and embryo development, but also contain food sources for the developing organism. AN are found in the oocytes of several species of wasps, and also in nematodes, other insects, and mammalian embryonic cells. [15] Bilinski and colleagues, in studying AN in Chrysis ignita, have shed light on the possible function of such accessory nuclei. They believe that AN have evolved independently of the rest of the wasp, so they can be used to genetically identify closely related species of chrysidid. [15] Further research may give us insight into the complexity of AN and its role in oocyte compartmentalization – as well as its importance for early embryonic development. [15]

Cajal bodies homologues

ANs form by budding off the nuclear envelope of the oocyte. They contain structures homologous Cajal Bodies, which are dense inclusions containing proteins and snRNPs. Bilinski and his colleagues have demonstrated that these bodies contain proteins and survival factors essential for the Hymenopteran development, such as survival of motor neuron (SMN) protein. They conjecture that this feature may be characteristic of all Hymenopterans, but further research is required to confirm this. [16]

Mitochondrial phylogeny

The ignita species group of the genus Chrysis includes over 100 cuckoo wasp species. [17] They all live the same parasitic life cycle and are morphologically indistinguishable. The lack of robust morphological features has hindered the construction of the phylogeny of these species of cuckoo wasp. [17] To solve this problem, researchers in Estonia have collected and analyzed the mitochondrial sequences of 41 ingroup and 6 outgroup taxa. By using two simultaneous Bayesian sequence alignment methods, they were able to reconstruct the ignita phylogeny. [17] Their phylogenetic analysis was backed up by maximum-parsimony and maximum-likelihood analyses and formed well-supported and defined clades. [17] Their results suggest that several taxa that are currently grouped together under subspecies may in fact be separate species. This phylogenetic approach will be helpful for further study of not only Chrysis ignita, but other chrysidids.

Anal teeth and phylogeny

The vast diversity of the cuckoo wasp family, Chrysididae, includes thousands of species, which have individually adapted to their environment and evolved tools uniquely suited to their survival and parasitic activity. This morphological diversity makes it difficult to classify the species. Another breakthrough came through the use of mitochondrial and rRNA sequencing alignment. A group in Germany has identified anal teeth as an early adaptive differentiation, which has potential to be used in phylogenetic reconstruction. [18]

Chemical mimicry

Host-parasite interactions are prime examples of evolutionary arms races. The host evolves methods of detecting the parasite, and the parasite counters by evolving methods of evasion. It has been reported in some specialized Chrysis species that the cuckoo wasp chemically camouflages itself when infiltrating the nest of its host. Field observations indicate that the cuckoo wasp is only attacked when the host wasp visually recognizes it. [19] If the cuckoo wasp can make it into the nest in the dark, research has shown that it can disguise itself chemically by secreting saturated and unsaturated hydrocarbons to match the scent profile of the host wasp. In these situations, even when the host wasp encounters the cuckoo wasp head on in the dark, the cuckoo wasp remains undetected. [19]

Related Research Articles

<span class="mw-page-title-main">Hymenoptera</span> Order of insects comprising sawflies, wasps, bees, and ants

Hymenoptera is a large order of insects, comprising the sawflies, wasps, bees, and ants. Over 150,000 living species of Hymenoptera have been described, in addition to over 2,000 extinct ones. Many of the species are parasitic. Females typically have a special ovipositor for inserting eggs into hosts or places that are otherwise inaccessible. This ovipositor is often modified into a stinger. The young develop through holometabolism —that is, they have a wormlike larval stage and an inactive pupal stage before they mature.

<span class="mw-page-title-main">Ovipositor</span> Anatomical structure for laying eggs

The ovipositor is a tube-like organ used by some animals, especially insects, for the laying of eggs. In insects, an ovipositor consists of a maximum of three pairs of appendages. The details and morphology of the ovipositor vary, but typically its form is adapted to functions such as preparing a place for the egg, transmitting the egg, and then placing it properly. For most insects, the organ is used merely to attach the egg to some surface, but for many parasitic species, it is a piercing organ as well.

<span class="mw-page-title-main">Kleptoparasitism</span> Type of animal feeding strategy

Kleptoparasitism is a form of feeding in which one animal deliberately takes food from another. The strategy is evolutionarily stable when stealing is less costly than direct feeding, such as when food is scarce or when victims are abundant. Many kleptoparasites are arthropods, especially bees and wasps, but including some true flies, dung beetles, bugs, and spiders. Cuckoo bees are specialized kleptoparasites which lay their eggs either on the pollen masses made by other bees, or on the insect hosts of parasitoid wasps. They are an instance of Emery's rule, which states that insect social parasites tend to be closely related to their hosts. The behavior occurs, too, in vertebrates including birds such as skuas, which persistently chase other seabirds until they disgorge their food, and carnivorous mammals such as spotted hyenas and lions. Other species opportunistically indulge in kleptoparasitism.

<span class="mw-page-title-main">Sawfly</span> Suborder of insects

Sawflies are the insects of the suborder Symphyta within the order Hymenoptera, alongside ants, bees, and wasps. The common name comes from the saw-like appearance of the ovipositor, which the females use to cut into the plants where they lay their eggs. The name is associated especially with the Tenthredinoidea, by far the largest superfamily in the suborder, with about 7,000 known species; in the entire suborder, there are 8,000 described species in more than 800 genera. Symphyta is paraphyletic, consisting of several basal groups within the order Hymenoptera, each one rooted inside the previous group, ending with the Apocrita which are not sawflies.

<span class="mw-page-title-main">Apocrita</span> Suborder of insects containing wasps, bees, and ants

Apocrita is a suborder of insects in the order Hymenoptera. It includes wasps, bees, and ants, and consists of many families. It contains the most advanced hymenopterans and is distinguished from Symphyta by the narrow "waist" (petiole) formed between the first two segments of the actual abdomen; the first abdominal segment is fused to the thorax, and is called the propodeum. Therefore, it is general practice, when discussing the body of an apocritan in a technical sense, to refer to the mesosoma and metasoma rather than the "thorax" and "abdomen", respectively. The evolution of a constricted waist was an important adaption for the parasitoid lifestyle of the ancestral apocritan, allowing more maneuverability of the female's ovipositor. The ovipositor either extends freely or is retracted, and may be developed into a stinger for both defense and paralyzing prey. Larvae are legless and blind, and either feed inside a host or in a nest cell provisioned by their mothers.

<span class="mw-page-title-main">Ichneumonoidea</span> Superfamily of wasps

The superfamily Ichneumonoidea contains one extinct and three extant families, including the two largest families within Hymenoptera: Ichneumonidae and Braconidae. The group is thought to contain as many as 100,000 species, many of which have not yet been described. Like other parasitoid wasps, they were long placed in the "Parasitica", variously considered as an infraorder or an unranked clade, now known to be paraphyletic.

<span class="mw-page-title-main">Parasitoid wasp</span> Group of wasps

Parasitoid wasps are a large group of hymenopteran superfamilies, with all but the wood wasps (Orussoidea) being in the wasp-waisted Apocrita. As parasitoids, they lay their eggs on or in the bodies of other arthropods, sooner or later causing the death of these hosts. Different species specialise in hosts from different insect orders, most often Lepidoptera, though some select beetles, flies, or bugs; the spider wasps (Pompilidae) exclusively attack spiders.

<span class="mw-page-title-main">Cuckoo wasp</span> Family of insects

Commonly known as cuckoo wasps or emerald wasps, the hymenopteran family Chrysididae is a very large cosmopolitan group of parasitoid or kleptoparasitic wasps, often highly sculptured, with brilliant metallic colors created by structural coloration. They are most diverse in desert regions of the world, as they are typically associated with solitary bee and wasp species, which are also most diverse in such areas. Their brood parasitic lifestyle has led to the evolution of fascinating adaptations, including chemical mimicry of host odors by some species.

<span class="mw-page-title-main">Chrysidinae</span> Subfamily of wasps

The subfamily Chrysidinae contains those species that are most commonly recognized as cuckoo wasps, being by far the largest and most familiar subfamily. The group contains 3000 species with 48 genera worldwide. They are highly sculptured, with brilliantly metallic-colored bodies, covering the entire spectrum, but primarily blues and greens.

<span class="mw-page-title-main">Leucospidae</span> Group of wasps

The Leucospidae are a specialized group of wasps within the superfamily Chalcidoidea, that are ectoparasitoids of aculeate wasps or bees. They are typically mimics of bees or stinging wasps, often black with yellow, red, or white markings, sometimes metallic, with a robust mesosoma and very strong sculpturing. The hind femora are often greatly enlarged, with a row of teeth or serrations along the lower margin as in Chalcididae. The wing has a longitudinal fold. The female ovipositor is sometimes short, but if not, it is recurved and lies along the dorsal side of the metasoma, a unique feature. The males are also unusual, in the fusion of many of the metasomal segments to form a capsule-like "carapace".

<span class="mw-page-title-main">Wasp</span> Group of insects

A wasp is any insect of the narrow-waisted suborder Apocrita of the order Hymenoptera which is neither a bee nor an ant; this excludes the broad-waisted sawflies (Symphyta), which look somewhat like wasps, but are in a separate suborder. The wasps do not constitute a clade, a complete natural group with a single ancestor, as bees and ants are deeply nested within the wasps, having evolved from wasp ancestors. Wasps that are members of the clade Aculeata can sting their prey.

<i>Chrysis inaequalis</i> Species of wasp

Chrysis inaequalis is a species of cuckoo wasps. The species occurs in Central and Southern Europe and in the Near East. The head and the thorax are shiny metallic blue-green, while the abdomen is red. Adults grow up to 5–10 millimetres (0.20–0.39 in) long and can be encountered from late June to mid September, especially flying on sun-exposed walls, on rocks and on dead wood.

<i>Chrysis viridula</i> Species of wasp

Chrysis viridula is a Western Palearctic species of cuckoo wasp, first described by Carl Linnaeus in 1761. Chrysis viridula is included in the genus Chrysis, and the family Chrysididae. It is a parasitoid of a number of species of eumenid wasp, mainly those in the genus Odynerus.

<i>Odynerus spinipes</i> Species of wasp

Odynerus spinipes, the spiny mason wasp, is a species of potter wasp from western Europe. It is the type species of the genus Odynerus, being first described by Carl Linnaeus in his landmark 1758 10th edition of Systema Naturae.

<i>Chrysura simplex</i> Species of wasp

Chrysura simplex is a species of cuckoo wasps, insects in the family Chrysididae.

<i>Chrysis ruddii</i> Species of wasp

Chrysis ruddii, the ruby-tailed wasp, is a species of cuckoo wasps, an insects in the family Chrysididae.

<i>Chrysis angustula</i> Species of wasp

Chrysis angustula is a species of cuckoo wasps, insects in the family Chrysididae.

<i>Omalus aeneus</i> Species of wasp

Omalus aeneus is a species of cuckoo wasps belonging to the family Chrysididae.

<i>Omalus biaccinctus</i> Species of wasp

Omalus biaccinctus is a species of cuckoo wasps belonging to the family Chrysididae.

<i>Chrysis angolensis</i> Species of wasp

Chrysis angolensis is a species of cuckoo wasp in the family Chrysididae, found throughout much of the world. It has been recently recorded as being introduced to French Polynesia. The species is a parasite of mud dauber nests, especially the black and yellow mud dauber Sceliphron caementarium.

References

  1. 1 2 3 4 Paukkunen, Juho; Berg, Alexander; Soon, Villu; Ødegaard, Frode; Rosa, Paolo (23 December 2015). "An illustrated key to the cuckoo wasps (Hymenoptera, Chrysididae) of the Nordic and Baltic countries, with description of a new species". ZooKeys (548): 1–116. doi: 10.3897/zookeys.548.6164 . PMC   4714362 . PMID   26798322.
  2. 1 2 Paukkunen, Juho; Pöyry, Juha; Kuussaari, Mikko (January 2018). "Species traits explain long-term population trends of Finnish cuckoo wasps (Hymenoptera: Chrysididae)". Insect Conservation and Diversity. 11 (1): 58–71. doi:10.1111/icad.12241. hdl: 10138/237259 .
  3. 1 2 3 Pauli, Thomas; Castillo-Cajas, Ruth F.; Rosa, Paolo; Kukowka, Sandra; Berg, Alexander; van den Berghe, Eric; Fornoff, Felix; Hopfenmüller, Sebastian; Niehuis, Manfred; Peters, Ralph S.; Staab, Michael; Strumia, Franco; Tischendorf, Stefan; Schmitt, Thomas; Niehuis, Oliver (April 2019). "Phylogenetic analysis of cuckoo wasps (Hymenoptera: Chrysididae) reveals a partially artificial classification at the genus level and a species-rich clade of bee parasitoids: Phylogeny and host associations of cuckoo wasps". Systematic Entomology. 44 (2): 322–335. doi:10.1111/syen.12323.
  4. 1 2 "Chrysis ignita Linnaeus, 1761". GBIF. Retrieved 20 March 2023.
  5. 1 2 3 4 5 6 7 8 9 Agnoli G.L. & Rosa P., Chrysis.net website, interim version 20-Sep-2013 , URL: http://www.chrysis.net/
  6. ↑ Carpenter, James M. "What Do We Know about Chrysidoid (Hymenoptera) Relationships?" Zoologica Scripta 28.1-2 (1999): 215-31.
  7. ↑ "What's That Insect?, Ruby-tailed Wasp | National Insect Week." Royal Entomological Society. N.p., n.d. Web. 16 Oct. 2014.
  8. ↑ Agnoli G.L. & Rosa P., 2014: Chrysis ignita Linnaeus, 1758. In: Chrysis.net Database of the Italian Chrysididae, interim version 10 October 2014 vv. URL: http://www.chrysis.net/database/
  9. 1 2 3 4 5 Kimsey, L. S. & Bohart, R. 1991 (1990). The Chrysidid Wasps of the World. Oxford University Press, New York.
  10. ↑ "Chrysis ignita (Linnaeus, 1758)." BWARS. Bees, Wasps & Ants Recording Society, n.d. Web.
  11. ↑ Tormos, J., K. V. Krombein, J. D. Asís, and S. F. Gayubo. "A Systematic Study of Larvae of Chrysidini (Hymenoptera: Chrysididae)." Annals of the Entomological Society of America 94.6 (2001): 809-34.
  12. 1 2 Malyshev S.J., 1911 - Zur biologie der Odynerus Arten und ihre Parasiten. (Chrysis ignita p. 36-39, fig. 16). Horae Societatis Entomologicae Rossicae, XL: 1-54. [in Russian with German summary]
  13. ↑ Agnoli, Gian Luca; Rosa, Paolo. "Chrysis ignita Linnaeus, 1758". Chrysis.net. Retrieved 20 March 2023.
  14. ↑ Kunz, Peter X. (1994). Die Goldwespen (Chrysididae) Baden-Württembergs : Taxonomie, Bestimmung, Verbreitung, Kartierung und Ökologie : mit einem Bestimmungsschlüssel für die deutschen Arten. Karlsruhe: Landesanstalt für Umweltschutz Baden-Württemberg. ISBN   3-88251-192-3.
  15. 1 2 3 Jaglarz, Mariusz K., Malgorzata Kloc, and Szczepan M. Bilinski. "Accessory Nuclei in Insect Oogenesis: In Search of the Function of Enigmatic Organelles." The International Journal of Developmental Biology 52.2-3 (2008): 179-85.
  16. ↑ Jaglarz, Mariusz K., Szczepan M. Bilinski, and M. Kloc. "Assembly and Breakdown of Cajal Bodies in Accessory Nuclei of Hymenoptera." Differentiation 73.2-3 (2005): 99-108.
  17. 1 2 3 4 Soon, Villu, and Urmas Saarma. "Mitochondrial Phylogeny of the Chrysis ignita (Hymenoptera: Chrysididae) Species Group Based on Simultaneous Bayesian Alignment and Phylogeny Reconstruction."Molecular Phylogenetics and Evolution 60.1 (2011): 13-20.
  18. ↑ Niehuis, Oliver, and Johann-Wolfgang Wägele. "Phylogenetic Analysis of the Mitochondrial Genes LSU RRNA and COI Suggests Early Adaptive Differentiation of Anal Teeth in Chrysidine Cuckoo Wasps (Hymenoptera: Chrysididae)." Molecular Phylogenetics and Evolution 30.3 (2004): 615-22.
  19. 1 2 Strohm, Erhard, Johannes Kroiss, Gudrun Herzner, Claudia Laurien-Kehnen, Wilhelm Boland, Peter Schreier, and Thomas Schmitt. "A Cuckoo in Wolves' Clothing? Chemical Mimicry in a Specialized Cuckoo Wasp of the European Beewolf (Hymenoptera, Chrysididae and Crabronidae)." Frontiers in Zoology 5.1 (2008): 2.
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