dcsimg

Lifespan, longevity, and ageing

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Maximum longevity: 8 years (wild)
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Reproduction

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Prior to the onset of breeding, males will develop a reproductive phenotype, including blue eyes, red throats, and red fore-bellies. During the breeding season, a male will leave the shoal and settle on the bottom in shallow water, where he will construct a nest and establish a territory. The males are are generally not monogamous, and a male often tries to lead numerous females into his nest to lay eggs. Afterward, he will fertilize all the eggs at once.

Males attract females with zig-zag-like courtship dances, and females respond with a form of dancing, as well as a "head-up" posture. The male will then lead the female to his nest, lying on the substrate next to the entrance to signify that she may enter and lay her eggs. Females lay their eggs in the male’s nest and then leave the male alone to attend to the eggs until they hatch. Once eggs are fertilized, they may take five to ten days to hatch, depending on the temperature of the water. The male nesting cycle consists of a sexual phase for 1 to 4 days, and then a parental phase after the eggs are fertilized.

Mating System: polygynous

Threespine sticklebacks breed in sloughs, ponds, rivers, lakes, drainage canals, marshes, tidal creeks and sublittoral zones of the sea. Individuals reach sexual maturity at between 1 and 2 years of age, and breeding occurs annually from late April to July.

Breeding interval: Threespine stickleback generally breed once yearly

Breeding season: late April to July

Range gestation period: 5 to 10 days.

Average time to independence: 2 weeks.

Range age at sexual or reproductive maturity (female): 1 to 2 years.

Range age at sexual or reproductive maturity (male): 1 to 2 years.

Key Reproductive Features: iteroparous ; seasonal breeding ; gonochoric/gonochoristic/dioecious (sexes separate); sexual ; fertilization (External ); oviparous

Once males shift to their parental phase, they provide all the care for their young. This includes fanning eggs with their pectoral fins to provide oxygen for the developing embryos and protecting them from predators. They also convert the nest into a nest pit, which consists of tangled vegetation where newly hatched fry can hide and rest. The males typically defend the fry up to two weeks after hatching. Paternal care has been identified as an important social factor in threespine stickleback development and learning. Sticklebacks with no paternal contact tend to fail avoiding predators later in life. These anti-predator behaviors may be stimulated at an early age as stickleback fathers chase and catch their fry when they first emerge from the nest.

Parental Investment: male parental care ; pre-hatching/birth (Provisioning: Male, Protecting: Male); pre-weaning/fledging (Provisioning: Male, Protecting: Male); pre-independence (Provisioning: Male, Protecting: Male)

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Keith Pecor, The College of New Jersey
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Renee Mulcrone, Special Projects
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Behavior

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Threespine sticklebacks rely on visual cues for mating behavior. Females tend to be attracted to more reddish coloring of males during mating seasons. They also use olfactory signals to detect the presence of conspecifics, prey, and predators. Like many other fish, threespine sticklebacks use alarm cues to avoid predation and sex pheromones during breeding. Lab-raised sticklebacks have been found to rely heavily on olfactory cues of kinship, habitat and diet, and shoal size. However, the sensory organs and pathways utilized in this communication are not well understood.

Communication Channels: visual ; chemical

Other Communication Modes: pheromones

Perception Channels: visual ; tactile ; chemical

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Conservation Status

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The unarmored threespine stickleback, Gasterosteus aculeatus williamsoni, a subspecies found in California, are listed as endangered in the United States.

US Federal List: endangered; no special status

CITES: no special status

State of Michigan List: no special status

IUCN Red List of Threatened Species: least concern

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Life Cycle

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Once eggs are fertilized, they take between 5 and 10 days to hatch, depending on the temperature of the water. Upon hatching, threespine stickleback larvae are about 4 mm in length. The larvae will continue to grow by absorption of the yolk, which they will completely consume about four days after hatching. Approximately nine days after hatching, the larvae reach a length of about 8 mm and assume the shape of the adult fish. This is the juvenile stage, in which the immature young become independent of their father. Juveniles become adults when they reach sexual maturity, which is usually within 1 to 2 years of hatching.

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Benefits

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Threespine sticklebacks have been widely studied in terms of speciation and evolutionary history because of their phylogeny and adaptive radiations. Their abundance and the relative ease to cross, raise, and maintain in the lab make them an excellent animal model for a variety of studies. Threespine sticklebacks have also served as subjects in research on environmental effects since they are considered bioindicators.

Positive Impacts: research and education

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Associations

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Threespine sticklebacks have many predators and are thus an important source of food for many different animals. They also act as predators for benthic invertebrates, such as amphipods and insect larvae.

Commensal/Parasitic Species:

  • tapeworm (Schistocephalus solidus)
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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Keith Pecor, The College of New Jersey
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Trophic Strategy

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Threespine sticklebacks are generalist carnivores and prey on limnetic and littoral invertebrates. Limnetic ecotypes in lentic environments feed on zooplankton, while benthic ecotypes feed on bottom-dwelling invertebrates in the littoral zone. Common benthic prey items include crustaceans (Amphipoda) and larval insects (Chironomidae). Threespine stickleback exhibit a predation cycle that consists of search, pursuit, attack, and capture components.

Animal Foods: eggs; insects; aquatic or marine worms; aquatic crustaceans; zooplankton

Foraging Behavior: stores or caches food

Primary Diet: carnivore (Insectivore , Eats non-insect arthropods, Vermivore); planktivore

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Distribution

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The threespine stickleback fish (Gasterosteus aculeatus) are in marine, brackish and coastal freshwater habitats of the northern hemisphere. They are found in boreal and temperate regions of the northern hemisphere and in marine waters and lowland freshwater habitats in the Atlantic and Pacific basins.

In the Atlantic Ocean, threespine sticklebacks are distributed from the Iberian Peninsula through the British Isles to Iceland and southern Greenland, and south along the east coast of North America to Chesapeake Bay. Freshwater populations are found throughout most of this range, but do not go farther south than Maine, USA. Freshwater populations are also distributed along the coast of the Mediterranean and in inland waters across Eastern Europe to the Baltic Sea.

In the Pacific Ocean, threespine sticklebacks are found from Baja California, Mexico northward along the coast of North America, across the Bering Strait, and then along the coast of mainland Asia and Japan to the southwest coast of Korea. Marine and freshwater populations are found in Japan, but the limit of marine populations in Asia is unclear. Freshwater populations are restricted to coastal areas in both Asia and North America.

Biogeographic Regions: nearctic (Native ); palearctic (Native ); atlantic ocean (Native ); pacific ocean (Native )

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Habitat

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Gasterosteus aculeatus occupy a wide range of habitats. They have been found in small, ephemeral streams in southern California and in more permanent flowing waters of variable sizes. These fish do not tolerate high-gradient streams, and they are rarely found in habitats more than a few hundred meters above sea level. In freshwater lakes, they are divided into benthic and limnetic ecotypes. Benthic environments include shallow, relatively eutrophic lakes or the littoral zone of deeper lakes. Limnetic ecotypes are typically found in the water column of deep oligotrophic lakes. Marine fish inhabit the open ocean.

Habitat Regions: temperate ; saltwater or marine ; freshwater

Aquatic Biomes: pelagic ; benthic ; lakes and ponds; rivers and streams; coastal ; brackish water

Other Habitat Features: estuarine ; intertidal or littoral

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Keith Pecor, The College of New Jersey
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Renee Mulcrone, Special Projects
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Life Expectancy

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Lifespans of threespine sticklebacks have been recorded in a large number of studies, but the results vary. A definitive pattern for the lifespan has not been determined. Threespine sticklebacks can live to approximately five years in the laboratory. One individual reached eight years of age in captivity.

Range lifespan
Status: captivity:
8 (high) years.

Average lifespan
Status: captivity:
5 years.

Average lifespan
Status: captivity:
5 years.

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Morphology

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Physical description varies widely with age and habitat. In general, threespine sticklebacks tend to be streamlined and less than 10 cm long (usually from 3 to 8 cm). Freshwater populations vary in body shape, depending on the habitat they occupy. Limnetic ecotypes tend to have slender bodies with narrow mouths, long snouts, and large eyes. Benthic ecotypes tend to be deep-bodied, with a wide, terminal gape.

The fish can have a robust set of spines, a pelvic girdle, and numerous lateral bony plates (up to thirty or more on each side), but the extent of these features varies by population. Dorsal and pelvic spines vary in number, placement, and length, and the spines tend to be longer in populations that co-occur with predatory fishes. The pelvic girdle consists of a bilateral structure with an anterior process that has an ascending branch on each side, a posterior process and a spine and fin ray. The abdomen is ringed in bony armor. Marine fish almost always possess a fully developed pelvic girdle and a full complement of bony lateral plates. However, many freshwater populations have reduced armor plates and pelvic girdles, and some populations have lost these features entirely.

Although body color also varies among populations, threespine sticklebacks are generally cryptic, with brown-to-green barring above and paler coloring below. As males approach reproductive condition, they become less cryptic, and their eyes become an iridescent blue. In some populations, red coloration may expand onto the flanks behind the pectoral fin.

Range length: 3 to 8 cm.

Average length: 5 cm.

Other Physical Features: ectothermic ; heterothermic ; bilateral symmetry

Sexual Dimorphism: sexes alike; sexes colored or patterned differently; male more colorful

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Keith Pecor, The College of New Jersey
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Renee Mulcrone, Special Projects
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Associations

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Threespine sticklebacks are small, abundant, and slow swimmers, all of which combine to make them suitable prey for many different predators. However, they have evolved several predator defenses in their morphology and behavior. Anti-predator morphology includes dorsal spines, bony lateral plates, and a pelvic girdle that consists of a pair of anterior processes with ascending branches, posterior processes and pelvic spines. Behavioral responses to predation risk include schooling, remaining close to protective cover, and predator inspection. Anti-predator morphology and behaviors tend to be more well-developed in fish from environments that contain predators.

Known predators of threespine sticklebacks include fish in the families Percidae, Esocidae, and Salmonidae. Some lakes in Alaska and British Columbia have been stocked with rainbow trout (Oncorhynchus mykiss) and silver salmon (Oncorhynchus kisutch) for game, and these fish prey on sticklebacks in those lakes. Avian piscivores that prey on stickleback fish include loons (Gaviiformes), grebes (Podicipediformes), the common merganser (Mergus merganser), herons (Ardeidae), and kingfishers (Alcedinidae). Piscivorous macroinvertebrates, such as dragonfly naiads (Odonata) and beetles (Coleoptera) feed on eggs, fry and juvenile sticklebacks. Leeches (Hirudinea) prey on stickleback eggs and have also been found to consume adult sticklebacks stuck in traps.

Known Predators:

  • perch, (Percidae)
  • trout and salmon, (Salmonidae)
  • pike, (Esocidae)
  • loons, (Gaviiformes)
  • grebes, (Podicipediformes)
  • common merganser, (Mergus merganser)
  • herons, (Ardeidae)
  • kingfishers, (Alcedinidae)
  • dragonflies, (Odonata)
  • beetles, (Coleoptera)
  • leeches, (Hirudinea)

Anti-predator Adaptations: cryptic

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Wood, S. 2011. "Gasterosteus aculeatus" (On-line), Animal Diversity Web. Accessed April 27, 2013 at http://animaldiversity.ummz.umich.edu/site/accounts/information/Gasterosteus_aculeatus.html
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Susan Wood, The College of New Jersey
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Keith Pecor, The College of New Jersey
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Renee Mulcrone, Special Projects
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Biology

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This stickleback is an active fish that forms schools (5). Marine three-spined sticklebacks are migratory, whereas freshwater forms tend to be resident (they stay in the same area for life) (2). Spawning occurs in early spring and summer. The male builds a hollow nest with seaweeds or aquatic plants. After much cajoling by the male, the female lays her eggs inside the nest and the male takes over parental duties, guarding the fertilised eggs and fanning them with his fins to provide them with oxygen (4). The young sticklebacks stay within the safety of the nest until they have absorbed their yolk sacs; they then enter the water where they initially live on plankton (2). After a while they begin to feed on worms, crustaceans, aquatic insects, small fishes and even the eggs and fry of their own species (5).
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Conservation

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Conservation action has not been targeted at this common species.
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Description

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The stickleback is a well-known fish, and is the archetypal 'tiddler', the first small fish caught by many school children (4). It is a small, beautifully streamlined, torpedo shaped fish, with a broad tail fin. Although most individuals tend to measure between 4 and 6 cm in length (2), some marine sticklebacks may grow to 10 cm (3). The common name derives from the most unique feature of these fish, the presence of two to four, but typically three, sharp spines on the back in front of the dorsal fin (3). The sides of this stickleback are usually covered with large bony plates; this armour is more developed on individuals living in the sea than freshwater sticklebacks (2). The back is dark grey, greyish or bluish-green, and the flanks are silvery (2). During the spawning season, males develop a metallic sheen and a prominent bright orange or red colouration on the front part of the underside (2).
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Habitat

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Both marine and freshwater forms of this fish are known (2). The freshwater form is found in well-vegetated sites that typically have muddy or sandy bottoms. In the sea they are found only in coastal areas and juveniles are associated with drifting patches of seaweed. This species is also common in estuaries (5).
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Range

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This widespread species is found throughout Britain and continental Europe from the Iberian Peninsula, the Black Sea and Italy in the south, reaching as far north as Iceland, Norway and the White Sea in Russia (2). Elsewhere it occurs in North Africa, Iran, the North Pacific, and the North Atlantic (5).
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Status

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Common and widespread in Britain (3).
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Threats

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This species is not currently threatened.
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Brief Summary

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Three-spined sticklebacks can live in fresh as well as salt water. Most spend the winter in coastal waters or river mouths. They migrate in the spring to inland waters where they make a nest and lay eggs. The male has to work hard. He builds the nest, defends his territory against other males, lures the females with a complicated zigzag dance, fans the eggs with oxygen-rich water using his fins and protects the eggs and later the young sticklebacks with all its might from voracious predators.
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Brief Summary

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The threespine stickleback (Gasterosteus aculeatus) is a species of fish in the family Gasterosteidae, which includes five genera and 15 other species. The threespine stickelback is small, between 4-6 cm, and is found in a circumpolar distribution that includes northern Europe, northern Asia and North America. It has also been introduced to central and southern Europe. Threespine sticklebacks are primarily and historically anadromous marine fish that feed on plankton for most of their adult lives in coastal waters and return to freshwater to mate and lay eggs. Threespine sticklebacks do not have scales, but have bony armor plates along their sides. In addition to the marine forms, threespine sticklebacks also exist in freshwater forms found in landlocked lakes. These many freshwater populations are thought to have derived from migratory anadromous G. aculeatus in many independent events, such as marine individuals permanently moving into a freshwater area or getting caught in land-locked lakes after the ice age, and subsequently adapting to an entirely freshwater existence. Freshwater threespine sticklebacks have notably reduced numbers of lateral armor plates as compared to marine populations and also show huge morphological diversity among different populations, so much that some populations living in the same lake do not interbreed. Gasterosteus aculeatus has contributed much to the study of species formation and are a research organism for evolutionary biologists and geneticists studying adaptation to new environments. Currently the IUCN (International Union for Conservation of Nature) recognizes three subspecies of threespine stickleback: Gasterosteus aculeatus aculeatus; G.a. williomsoni, the unarmored threespine stickeback; and G. a. santaeannae, the Santa Ana stickleback, but some taxonomists would classify the sticklebacks inhabiting isolated lakes into many more subspecies. Although the species itself is abundant and in no threat of extinction, various populations that represent specific diversity are in danger of local extirpation. Froese and Pauly 2010; Hammerson et al 2012; Natureserve 2011; US Fish and Wildlife Service 2012; Wikipedia 4 January 2012; Wikipedia 6 February 2012)
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Diagnostic Description

provided by Fishbase
Distinguished uniquely from its congeners in Europe by having trunk and caudal peduncle covered by a complete series of 29-35 bony scutes. Other characters important to separate this species from other species of the genus include posterior edge of scutes crenulated and scutes forming a lateral keel on caudal peduncle. Scutes may be missing on posterior part of trunk in hybrid zone with Gasterosteus gymnurus and in some isolated freshwater populations of northeastern Europe (Ref. 59043). Identified by the 3 to 4 sharp, free spines before the dorsal fin, the pelvic fin reduced to a sharp spine and a small ray, and the series of plates along the sides of the body (Ref. 27547). Gill rakers long and slender, 17 to 25 on the first arch or strictly freshwater forms, 1 or 2 more in anadromous forms; lateral line with microscopic pores (Ref. 27547). The anadromous form is fully plated, with up to 37 plates on the sides and a rather pronounced keel on each side of the caudal peduncle (Ref. 27547). Dorsal spines separated from each other and from the soft-rayed fins, each spine having a reduced membrane attached to its posterior side; anal spine free from rest of the fin; posterior margin of pectorals nearly truncate; caudal truncate to slightly indented (Ref. 27547). Freshwater forms usually mottled brown or greenish; anadromous forms silvery green to bluish black (Ref. 27547). A few isolated populations are black (Ref. 27547). Sides usually pale; belly yellow, white or silvery (Ref. 27547). Fins pale; pectoral rays often have dark dots (Ref. 27547). Breeding males (except for black forms) become brilliant bluish or green with blue or green eyes, and the forward part of the body, especially the breast region, turns bright red or orange (Ref. 27547). Caudal fin with 12 rays (Ref. 2196).
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Recorder
Susan M. Luna
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Life Cycle

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Spawning behavior is similar for both freshwater and anadromous forms (Ref. 28966). Just before breeding, males become very territorial. The male builds a nest of plant-material glued together with spiggin, a protein produced in the kidney (Ref. 52349). Once a nest is built, the male entices the female into the nest by performing a courtship dance which is a series of zigzag movements (Ref. 1998). A receptive female follows the male who points the opening of the nest by posing above it with his head down. The female enters the nest, deposits up to a few hundred eggs, and is driven out by the male after eggs have been deposited. The male then enters the nest to fertilize the eggs. The male can choose to court another female to enter the nest and lay eggs before entering himself to fertilise the deposited eggs. Females may lay eggs in several nests over a period of several days or may be courted by the same male (Ref. 27547). The male guards and ventilates the eggs and young (Ref. 1998). During spawning season, males develop a bright orange to red belly and blue-green flank and eyes. Eggs hatch in 7-8 days. Anadromous forms usually die of exhaustion after spawning cycle. Freshwater individuals are able to complete several cycles within one year or sometimes over several years (Ref. 59043).
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Susan M. Luna
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Migration

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Anadromous. Fish that ascend rivers to spawn, as salmon and hilsa do. Sub-division of diadromous. Migrations should be cyclical and predictable and cover more than 100 km.
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Morphology

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Dorsal spines (total): 2 - 4; Dorsal soft rays (total): 10 - 14; Analspines: 1; Analsoft rays: 8 - 10; Vertebrae: 29 - 33
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Threats

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Least Concern (LC)
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Crispina B. Binohlan
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Trophic Strategy

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Shoaling species outside the breeding season, especially when young. Inhabits vegetated areas, usually over mud or sand (Ref. 5723). In the sea, confined to coastal waters. Forms schools. Eggs are found in nests constructed from plant material (Ref. 41678). Anadromous and nerito-pelagic (Ref. 58426). Feeds on worms, crustaceans, larvae and adult aquatic insects, drowned aerial insects, and small fishes; has also been reported to feed on their own fry and eggs (Ref. 1998). Length in freshwater is 8 cm while in saltwater is 11 cm (Ref. 35388). Preyed upon by American mergansers.
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Diagnostic Description

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Distinguished uniquely from congeners in Europe by the absence of scutes or lateral keel on caudal peduncle, except in few individuals from Sardinia. Differs further from congeners by the combination of the following characters: trunk lacking or with only 2-10 bony scutes; and scutes overlapping. Scutes may be more numerous and present on caudal peduncle in hybrid zone with Gaterosteus aculeatus (Ref. 59043).
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Armi G. Torres
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Life Cycle

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Males defend territories where they construct a nest on the bottom in relatively shallow areas. They excavate to make a depression where they bring plant materials, which are glued together with kidney secretions and covered by sand, leaving only the entrance distinct. Females are led to the nest to spawn then chased away. Males guard and fan eggs which hatch in about 10 days. Juveniles are protected for a few days, after which males abandon the nest.
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Threats

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Least Concern (LC)
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Biology

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Adults occur in fresh waters, estuaries and coastal seas (Ref. 4119). Anadromous, with numerous non-anadromous populations in brackish or pure freshwater, rarely in marine waters. In the sea, confined to coastal waters. In freshwater, adults prefer to live in small stream but may occur in a variety of habitats including lakes and large rivers (Ref. 59043). Inhabit shallow vegetated areas, usually over mud or sand (Ref. 5723). Form schools. Young associated with drifting seaweed (Ref. 12114, 12115). Juveniles move to the sea (anadromous populations) or to deeper, larger water bodies (freshwater populations) in July-August, forming large feeding schools (Ref. 59043). Feed on worms, crustaceans, larvae and adult aquatic insects, drowned aerial insects, and small fishes; has also been reported to feed on their own fry and eggs (Ref. 1998). Eggs are found in nests constructed from plant material (Ref. 41678). Males build, guard and aerate the nest where the eggs are deposited (Ref. 205). Maximum length in freshwater is 8 cm while in saltwater is 11 cm (Ref. 35388). Occasionally taken commercially in Scandinavia and processed into fishmeal and oil (Ref. 28219, 28964). Commonly used as a laboratory animal (Ref. 1998). A large bibliography is available at www.geocities.com/CapeCanaveral/Hall/1345/stickbibl.html.
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Biology

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Adults inhabit streams, lakes and ponds with slow to moderate current, clear water and sand bottom. In Mediterranean basin, commonly found in spring-fed water bodies and also occur in other habitats including brackish water. Feed predominantly on small invertebrates. Spawn in springs and brackish water. Males build, guard and aerate the nest where the eggs are deposited (Ref. 205). Locally rare or extirpated in several Mediterranean drainages. Size reaches up to about 10 cm SL (Ref. 59043).
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Importance

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fisheries: minor commercial; aquarium: public aquariums; price category: unknown; price reliability:
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Three-spined stickleback

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The three-spined stickleback (Gasterosteus aculeatus) is a fish native to most inland coastal waters north of 30°N. It has long been a subject of scientific study for many reasons. It shows great morphological variation throughout its range, ideal for questions about evolution and population genetics. Many populations are anadromous (they live in seawater but breed in fresh or brackish water) and very tolerant of changes in salinity, a subject of interest to physiologists. It displays elaborate breeding behavior (defending a territory, building a nest, taking care of the eggs and fry) and it can be social (living in shoals outside the breeding season) making it a popular subject of enquiry in fish ethology and behavioral ecology. Its antipredator adaptations, host-parasite interactions, sensory physiology, reproductive physiology, and endocrinology have also been much studied. Facilitating these studies is the fact that the three-spined stickleback is easy to find in nature and easy to keep in aquaria.

Description

This species can occasionally reach lengths of 8 cm (3.1 in), but lengths of 3–4 centimetres (1.2–1.6 in) at maturity are more common. The body is laterally compressed. The base of the tail is slender. The caudal fin has 12 rays. The dorsal fin has 10–14 rays; in front of it are the three spines that give the fish its name (though some individuals may have only two or four). The third spine (the one closest to the dorsal fin) is much shorter than the other two. The back of each spine is joined to the body by a thin membrane. The anal fin has eight to 11 rays and is preceded by a short spine. The pelvic fins consist of just a spine and one ray. All spines can be locked in an erect position, making the fish extremely hard to swallow by a predator. The pectoral fins are large, with 10 rays. The body bears no scales, but is protected by bony plates on the back, flanks, and belly. Only one ventral plate is present, but the number of flank plates varies greatly across the distribution range and across habitat types (see below); it is normally higher in marine populations (some freshwater populations may in fact lack lateral plates altogether).[2]

Dorsal coloration varies, but tends towards a drab olive or a silvery green, sometimes with brown mottling. The flanks and belly are silvery. In males during the breeding season, the eyes become blue and the lower head, throat, and anterior belly turn bright red. The throat and belly of breeding females can turn slightly pink. A few populations, however, have breeding males which are all black[3] or all white.[4]

Habitat and distribution

The three-spined stickleback is found only in the Northern Hemisphere, where it usually inhabits coastal waters or freshwater bodies. It can live in either fresh, brackish, or salt water. It prefers slow-flowing water with areas of emerging vegetation. It can be found in ditches, ponds, lakes, backwaters, quiet rivers, sheltered bays, marshes, and harbours.

In North America, it ranges along the East Coast from Chesapeake Bay to the southern half of Baffin Island and the western shore of Hudson Bay, and along the West Coast from southern California to the western shore of Alaska and the Aleutian Islands. It can be found throughout Europe between 35 and 70°N. In Asia, the distribution stretches from Japan and the Korean peninsula to the Bering Straits.

"
Distribution of Gasterosteus aculeatus (Three-spine stickleback) in the United States, from USGS NAS web site

Its distribution could be said to be circumpolar were it not for the fact that it is absent from the north coast of Siberia, the north coast of Alaska, and the Arctic islands of Canada.

Variation in morphology and distribution

"Gasterosteus

Three subspecies are currently recognized by the IUCN:

  • G. a. aculeatus is found in most of the species range, and is the subspecies most strictly termed the three-spined stickleback; its common name in Britain is the tiddler, although "tittlebat" is also sometimes used.
  • G. a. williamsoni, the unarmored threespine stickleback, is found only in North America; its recognised range is southern California, though isolated reports have been made of it occurring in British Columbia and Mexico;
  • G. a. santaeannae, the Santa Ana stickleback, is also restricted to North America.
The head of a threespine stickleback (G. aculeatus) reconstructed into a 3D mesh from a microCT scan. This individual was from a freshwater stream population on Vancouver Island, BC. Many stickleback traits can vary a great deal between freshwater populations, including the number of bony lateral plates, a few of which can be seen towards the posterior edge of this mesh, and the number and length of gill rakers and pharyngeal teeth, which can be see inside the mouth.

These subspecies actually represent three examples from the enormous range of morphological variation present within three-spined sticklebacks. These fall into two rough categories, the anadromous and the freshwater forms.

The anadromous form spends most of its adult life eating plankton and fish in the sea, and returns to freshwater to breed. The adult fish are typically between 6 and 10 cm long, and have 30 to 40 lateral armour plates along their sides. They also have long dorsal and pelvic spines. The anadromous form is morphologically similar all around the Northern Hemisphere, such that anadromous fish from the Baltic, the Atlantic and the Pacific all resemble each other quite closely.

Three-spined stickleback populations are also found in freshwater lakes and streams. These populations were probably formed when anadromous fish started spending their entire lifecycle in fresh water, and thus evolved to live there all year round. Freshwater populations are extremely morphologically diverse, to the extent that many observers (and some taxonomists) would describe a new subspecies of three-spined stickleback in almost every lake in the Northern Hemisphere. One consistent difference between freshwater populations and their anadromous ancestors is the amount of body armour, as the majority of freshwater fish only have between none and 12 lateral armour plates, and shorter dorsal and pelvic spines. However, also large morphological differences occur between lakes. One major axis of variation is between populations found in deep, steep-sided lakes and those in small, shallow lakes. The fish in the deep lakes typically feed in the surface waters on plankton, and often have large eyes, with short, slim bodies and upturned jaws. Some researchers refer to this as the limnetic form. Fish from shallow lakes feed mainly on the lake bed, and are often long and heavy bodied with relatively horizontal jaws and small eyes. These populations are referred to as the benthic form.

Since each watershed was probably colonised separately by anadromous sticklebacks, morphologically similar populations in different watersheds or on different continents are widely believed to have evolved independently. A unique population is found in the meromictic Pink Lake in Gatineau Park, Quebec.

One aspect of this morphological variation is that a number of lakes contain both a limnetic and a benthic type, and these do not interbreed with each other. Evolutionary biologists often define species as populations that do not interbreed with each other (the biological species concept), thus the benthics and limnetics within each lake would constitute separate species. These species pairs are an excellent example of how adaptation to different environments (in this case feeding in the surface waters or on the lake bed) can generate new species. This process has come to be termed ecological speciation. This type of species pair is found in British Columbia. The lakes themselves only contain three-spined sticklebacks and cutthroat trout, and all are on islands. Tragically, the pair in Hadley Lake on Lasqueti Island was destroyed in the mid-1980s by the introduction of a predatory catfish, and the pair in Enos Lake on Vancouver Island has started to interbreed and are no longer two distinct species.[5] The two remaining pairs are on Texada Island, in Paxton Lake and Priest Lake, and they are listed as Endangered in the Canadian Species at Risk Act.[6]

Other species pairs which consist of a well-armored marine form and a smaller, unarmored freshwater form are being studied in ponds and lakes in south-central Alaska that were once marine habitats such as those uplifted during the 1964 Alaska earthquake. The evolutionary dynamics of these species pairs are providing a model for the processes of speciation which has taken place in less than 20 years in at least one lake. In 1982, a chemical eradication program intended to make room for trout and salmon at Loberg Lake, Alaska, killed the resident freshwater populations of sticklebacks. Oceanic sticklebacks introduced through nearby Cook Inlet recolonized the lake. In just 12 years beginning in 1990, the frequency of the oceanic form dropped steadily, from 100% to 11%, while a variety with fewer plates increased to 75% of the population, with various intermediate forms making up another small fraction.[7] This rapid evolution is thought to be possible through genetic variations that confer competitive advantages for survival in fresh water when conditions shift rapidly from salt to fresh water. However, the actual molecular basis of this evolution still remains unknown.

Although sticklebacks are found in many locations around the coasts of the Northern Hemisphere and are thus viewed by the IUCN as species of least concern, the unique evolutionary history encapsulated in many freshwater populations indicates further legal protection may be warranted.[1]

Diet

In its different forms or stages of life, the three-spined stickleback can be a bottom-feeder (most commonly chironomid larvae) or a planktonic feeder in lakes or in the ocean; it can also consume terrestrial prey fallen to the surface.[8] It can cannibalize eggs and fry.[9]

Life history

"
Male stickleback with red throat and shiny blue eye

Many populations take two years to mature and experience only one breeding season before dying, and some can take up to three years to reach maturity. However, some freshwater populations and populations at extreme latitudes can reach maturity in only one year.

Reproduction

From late April, males and females move from deeper waters to shallow areas. There, each male defends a territory where he builds a nest on the bottom. He starts by digging a small pit. He then fills it with plant material (often filamentous algae), sand, and various debris which he glues together with spiggin, a proteinaceous substance secreted from the kidneys (the word spiggin comes from spigg, the Swedish name for the three-spined stickleback). He then creates a tunnel through the more or less spherical nest by swimming vigorously through it. Nest building typically takes 5–6 hours[10] though it may also be spread out over several days. After this, the male courts gravid females that pass by with a zigzag dance. He approaches a female by swimming very short distances left and right, and then swims back to the nest in the same way. If the female follows, the male often pokes his head inside the nest, and may swim through the tunnel. The female then swims through the tunnel as well, where she deposits 40–300 eggs. The male follows to fertilize the eggs. The female is then chased away by the male. For the duration of the eggs' development, the male will chase away other males and nongravid females. He may, however, court other gravid females (more than one batch of eggs can be deposited in the same nest).

The sequence of territorial courtship and mating behaviours was described in detail by Niko Tinbergen in a landmark early study in ethology. Tinbergen showed that the red colour on the throat of the territorial male acts as a simple sign stimulus, releasing aggression in other males and attracting females.[11] The red colouration may also be used by females as a way to assess male quality. Red colouration is produced from carotenoids found in the diet of the fish. As carotenoids cannot be synthesised de novo, the degree of colouration gives an indication of male quality (ability to find food), with higher-quality males showing more intense colouration. Also, males that bear fewer parasites tend to exhibit brighter red colours. Many studies have shown that females prefer males with brighter red colouration.[12][13][14][15] However, the response to red is not universal across the entire species,[16][17] with black throated populations often found in peat-stained waters.

The male takes care of the developing eggs by fanning them. He lines himself up with the entrance of the nest tunnel and swims on the spot. The movement of his pectoral fins creates a current of water through the nest, bringing fresh (well-oxygenated) water to the eggs. He does this not only during the day, but throughout the night, as well.[18] Fanning levels tend to increase until the eggs are about to hatch, which takes 7–8 days at 18–20 °C. Fanning levels also increase when the water is poorly oxygenated.[19] Towards the end of the egg development phase, the male often makes holes in the roof and near the rim of the nest, presumably to improve ventilation of the nest during fanning at a time when the eggs are more metabolically active. Once the young hatch, the male attempts to keep them together for a few days, sucking up any wanderers into his mouth and spitting them back into the nest. Afterwards, the young disperse and the nest is either abandoned by the male, or repaired in preparation for another breeding cycle.

In Nova Scotia, a form of three-spined stickleback departs from the usual pattern of parental care. Unlike other sticklebacks that nest on the substrate, Nova Scotian male sticklebacks build nests in mats of filamentous algae. Surprisingly, almost immediately after fertilization, the males disperse the eggs from the nest and resume soliciting females for eggs. Hence, there appears to have been a loss of parental care in this population. Because these males have reduced dorsal pigmentation, resulting a pearlescent white appearance, they have been dubbed "white sticklebacks". It is currently unknown whether they are a distinct species, or simply a morph of the common Atlantic stickleback.[20][21][22]

Infection with the cestode parasite Schistocephalus solidus causes a reduction in egg mass production or complete absence of eggs in female three-spined sticklebacks [23].

Cooperative behavior

Some evidence indicates the existence of cooperative behavior among three-spined sticklebacks, mainly cooperative predator inspection. Predator inspection appears to allow acquisition of information about the risk a potential predator presents, and may deter attack, with the cost being an increased chance of being attacked if the predator proves to be hungry.

Tit-for-tat strategy

Sticklebacks are known to cooperate in a tit-for-tat (TFT) strategy when doing predator inspection. The idea behind TFT is that an individual cooperates on the first move and then does whatever its opponent does on the previous move. This allows for a combination of collaborative (it starts by cooperating), retaliatory (punishes defection), and forgiving (respond to cooperation of others, even if they had defected previously) behavioral responses.[24] When three-spined sticklebacks approaching a live predator were provided with either a simulated cooperating companion or a simulated defecting one, the fish behaved according to tit-for-tat strategy, supporting the hypothesis that cooperation can evolve among egoists.[25]

Typically, sticklebacks operate in pairs. Individuals have partners with which they repeatedly perform pairwise predator inspection visits. Two reciprocal pairs per trial occur significantly more often than what was expected due to chance. These results provide further evidence for a tit-for-tat cooperation strategy in sticklebacks.[26]

Stickleback behavior is often cited as an archetypal example of cooperative behavior during predator inspection. Fish from three sites differing in predation risk inspected a model predator in pairs and reciprocated both cooperative moves and defections by the partner, but not on every opportunity.[27] Sticklebacks that originated in the two sites containing piscivorous fish were more likely to reciprocate following a cooperative move than following a defection. Individuals from higher-risk sites were generally more cooperative.[27] Individuals accompanied by a model companion show reciprocal moves of cooperation and defection in response to the model's movements about a third of the time. Both examples of stickleback behavior demonstrate the elements of a strategy of cooperation that may resemble tit-for-tat.[27]

Partner-dependence

The tit-for-tat cooperation strategy has been shown to be evident in sticklebacks. In addition, the size of a stickleback's partner fish may also be a factor in determining what a stickleback will do when both fish are faced with a predator. Two sticklebacks simultaneously presented to a rainbow trout, a predator much larger in size, will have differing risks of being attacked. Usually, the larger of the two sticklebacks has a higher risk of being attacked.[28] Individual sticklebacks are more likely to move closer to a trout (or some other predator) when a larger potential partner moves close to the trout than when a smaller partner approaches the trout.[28] Although both large and small partners behave similarly, a small partner's behavior affects the strategy of the test fish more than that of the large partner.[28] Regardless of whether it is alone or with a partner that cooperates, a larger fish will approach a predator more closely than does a smaller fish.[28] If a partner defects, then a stickleback's condition-factor (i.e. its ability to flee) determines how closely it approaches the predator rather than the stickleback's size.[28] Both the strategy and reaction to different-sized partners seem to be dependent on whether the partner cooperates or defects.

Sensory biology

"
A three-spined stickleback with stained neuromasts that form the lateral line system.

Sticklebacks have four colour photoreceptor cells in their retina, making them potentially tetrachromatic. They are capable of perceiving ultraviolet wavelengths of light invisible to the human eye and use such wavelengths in their normal behavioural repertoire.

Parasites

The three-spined stickleback is a known intermediate host for the hermaphroditic parasite Schistocephalus solidus, a tapeworm of fish and fish-eating birds.[29]

Genetics

Three-spined sticklebacks have recently become a major research organism for evolutionary biologists trying to understand the genetic changes involved in adapting to new environments. The entire genome of a female fish from Bear Paw Lake in Alaska was recently sequenced by the Broad Institute and many other genetic resources are available.[30] This population is under risk from the presence of introduced northern pike in a nearby lake.

References

  1. ^ a b NatureServe (2015). "Gasterosteus aculeatus". IUCN Red List of Threatened Species. 2015: e.T8951A76576912. doi:10.2305/IUCN.UK.2015-1.RLTS.T8951A76576912.en.
  2. ^ Froese, Rainer and Pauly, Daniel, eds. (2006). "Gasterosteus aculeatus" in FishBase. February 2006 version.
  3. ^ Reimchen, T.E. (1989). "Loss of nuptial colour in three-spined sticklebacks (Gasterosteus aculeatus)". Evolution. 43 (2): 450–460. doi:10.2307/2409219. JSTOR 2409219. PMID 28568546.
  4. ^ Haglund, T. R.; Buth, D. G.; Blouw, D. M. (1990). "Allozyme variation and the recognition of the "white stickleback"". Biochemical Systematics and Ecology. 18 (7–8): 559–563. doi:10.1016/0305-1978(90)90129-4.
  5. ^ Behm, J. E.; Ives, A. R.; Boughman, J. W. (2010). "Breakdown in Postmating Isolation and the Collapse of a Species Pair through Hybridization". The American Naturalist. 175 (1): 11–26. doi:10.1086/648559. PMID 19916869.
  6. ^ Canada – Species At Risk Act. dfo-mpo.gc.ca
  7. ^ Carroll, Sean B. (2006). The Making of the Fittest: DNA and the Ultimate Forensic Record of Evolution. W.W. Norton & Co. pp. 56–57. ISBN 978-0-393-06163-5.
  8. ^ Sánchez-Hernández, J. (2012). "Aplicación del análisis de los rasgos biológicos ("traits") de las presas para el estudio del comportamiento alimentario en peces bentófagos: el ejemplo del espinoso (Gasterosteus gymnurus Cuvier 1829)". Limnetica. 31 (1): 59–76.
  9. ^ Whoriskey, F. G.; FitzGerald, G. J. (1985). "Sex, cannibalism and sticklebacks". Behavioral Ecology and Sociobiology. 18 (1): 15–18. doi:10.1007/BF00299233 (inactive 2020-03-18).
  10. ^ van Iersel, J.J.A. (1953). "An analysis of the parental behaviour of the malethree-spined stickleback (Gasterosteus aculeatus L.)". Behaviour Supplement. 3 (3): 1–159. JSTOR 30039128.
  11. ^ Tinbergen, N. (1951) The study of instinct, Clarendon Press, Oxford.
  12. ^ Milinski, M.; Bakker, T. C. M. (1990). "Female sticklebacks use male coloration in mate choice and hence avoid parasitized males" (PDF). Nature. 344 (6264): 330–333. Bibcode:1990Natur.344..330M. doi:10.1038/344330a0.
  13. ^ McLennan, D. A.; McPhail, J. D. (1990). "Experimental investigations of the evolutionary significance of sexually dimorphic nuptial colouration in Gasterosteus aculeatus (L.): The relationship between male colour and female behaviour". Canadian Journal of Zoology. 68 (3): 482–492. doi:10.1139/z90-071.
  14. ^ Bakker, T. C. M.; Mundwiler, B. (1994). "Female mate choice and male red coloration in a natural three-spined stickleback (Gasterosteus aculeatus) population" (PDF). Behavioral Ecology. 5: 74–80. doi:10.1093/beheco/5.1.74.
  15. ^ Baube, C.L.; Rowland, W.J.; Fowler, J.B. (1995). "The mechanismsof colour-based mate choice in female threespine sticklebacks: hue, contrast and configurational cues". Behaviour. 132 (13/14): 979–996. doi:10.1163/156853995x00405. JSTOR 4535315.
  16. ^ McKinnon, J. S. (1995). "Video mate preferences of female three-spined sticklebacks from populations with divergent male coloration". Animal Behaviour. 50 (6): 1645–1655. doi:10.1016/0003-3472(95)80018-2.
  17. ^ Braithwaite, V. A.; Barber, I. (2000). "Limitations to colour-based sexual preferences in three-spined sticklebacks (Gasterosteus aculeatus)". Behavioral Ecology and Sociobiology. 47 (6): 413–416. doi:10.1007/s002650050684.
  18. ^ Reebs, S. G.; Whoriskey Jr., F. G.; Fitzgerald, G. J. (1984). "Diel patterns of fanning activity, egg respiration, and the nocturnal behavior of male three-spined sticklebacks, Gasterosteus aculeatus L. (f. trachurus)". Canadian Journal of Zoology. 62 (3): 329–334. doi:10.1139/z84-051.
  19. ^ Seventer, P. (1961). "A causal study of a displacement activity (fanning in Gasterosteus aculeatus L.)". Behaviour Supplement. 9: 1–170.
  20. ^ MacDonald, J. F.; Bekkers, J.; MacIsaac, S. M.; Blouw, D. M. (1995). "Intertidal Breeding and Aerial Development of Embryos of a Stickleback Fish (Gasterosteus)". Behaviour. 132 (15): 1183–1206. doi:10.1163/156853995x00522. JSTOR 4535330.
  21. ^ MacDonald, J. F.; MacIsaac, S. M.; Bekkers, J.; Blouw, D. M. (1995). "Experiments on Embryo Survivorship, Habitat Selection, and Competitive Ability of a Stickleback Fish (Gasterosteus) Which Nests in the Rocky Intertidal Zone". Behaviour. 132 (15): 1207–1221. doi:10.1163/156853995x00531.
  22. ^ Jamieson, I. G.; Blouw, D. M.; Colgan, P. W. (1992). "Field observations on the reproductive biology of a newly discovered stickleback (Gasterosteus)". Canadian Journal of Zoology. 70 (5): 1057–1063. doi:10.1139/z92-148.
  23. ^ Heins, David C.; Baker, John A. (February 2003). "Reduction of egg size in natural populations of threespine stickleback infected with a cestode macroparasite". Journal of Parasitology. 89 (1): 1–6. doi:10.1645/0022-3395(2003)089[0001:ROESIN]2.0.CO;2. PMID 12659295.
  24. ^ Nicholas B. Davies; John R. Krebs; Stuart A. West (2012-04-02). An introduction to behavioural ecology (4th ed.). Oxford: Wiley-Blackwell. ISBN 978-1-4051-1416-5.
  25. ^ Milinski, Manfred (1987). "TIT FOR TAT in sticklebacks and the evolution of cooperation". Nature. 325 (29): 433–435. Bibcode:1987Natur.325..433M. doi:10.1038/325433a0. PMID 3808044.
  26. ^ Milinski, Manfred; D. Pfluger; D. Kulling; R. Kettler (1990). "Do sticklebacks cooperate repeatedly in reciprocal pairs?". Behavioral Ecology and Sociobiology. 27 (1): 17–21. doi:10.1007/bf00183308.
  27. ^ a b c Huntingford, Felicity; John Lazarus; Brian Barrie; Sally Webb (1994). "A dynamic analysis of cooperative predator inspection in sticklebacks". Animal Behaviour. 47 (2): 413–423. doi:10.1006/anbe.1994.1055.
  28. ^ a b c d e Kulling, David; Manfred Milinski (1992). "Size-dependent predation risk and partner quality in predator inspection of sticklebacks". Animal Behaviour. 44 (5): 949–955. doi:10.1016/s0003-3472(05)80590-1.
  29. ^ Lobue, C. P.; Bell, M. A. (1993). "Phenotypic Manipulation by the Cestode Parasite Schistocephalus solidus of Its Intermediate Host, Gasterosteus aculeatus, the Threespine Stickleback". The American Naturalist. 142 (4): 725–35. doi:10.1086/285568. JSTOR 2462871. PMID 19425968.
  30. ^ "Stickleback Genome at ENSEMBL".
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Three-spined stickleback: Brief Summary

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The three-spined stickleback (Gasterosteus aculeatus) is a fish native to most inland coastal waters north of 30°N. It has long been a subject of scientific study for many reasons. It shows great morphological variation throughout its range, ideal for questions about evolution and population genetics. Many populations are anadromous (they live in seawater but breed in fresh or brackish water) and very tolerant of changes in salinity, a subject of interest to physiologists. It displays elaborate breeding behavior (defending a territory, building a nest, taking care of the eggs and fry) and it can be social (living in shoals outside the breeding season) making it a popular subject of enquiry in fish ethology and behavioral ecology. Its antipredator adaptations, host-parasite interactions, sensory physiology, reproductive physiology, and endocrinology have also been much studied. Facilitating these studies is the fact that the three-spined stickleback is easy to find in nature and easy to keep in aquaria.

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Diet

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Feeds on copepods, euphausiids, isopods, small fishes and fish eggs
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Muller, Y. (2004). Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. [Coastal fauna and flora of the Nord, Pas-de-Calais and Belgium: inventory]. <em>Commission Régionale de Biologie Région Nord Pas-de-Calais: France.</em> 307 pp. North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS)
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Distribution

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Hudson Bay to Chesapeake Bay
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Muller, Y. (2004). Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. [Coastal fauna and flora of the Nord, Pas-de-Calais and Belgium: inventory]. <em>Commission Régionale de Biologie Région Nord Pas-de-Calais: France.</em> 307 pp. North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS)
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Habitat

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Benthopelagic species found to depths of 27 m, inhabits vegetated areas over sand and mud bottoms.
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WoRMS Editorial Board
bibliographic citation
Muller, Y. (2004). Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. [Coastal fauna and flora of the Nord, Pas-de-Calais and Belgium: inventory]. <em>Commission Régionale de Biologie Région Nord Pas-de-Calais: France.</em> 307 pp. North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS)
Contributor
Mary Kennedy [email]

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WoRMS Editorial Board
bibliographic citation
Muller, Y. (2004). Faune et flore du littoral du Nord, du Pas-de-Calais et de la Belgique: inventaire. [Coastal fauna and flora of the Nord, Pas-de-Calais and Belgium: inventory]. <em>Commission Régionale de Biologie Région Nord Pas-de-Calais: France.</em> 307 pp. North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS) North-West Atlantic Ocean species (NWARMS)
Contributor
Mary Kennedy [email]