Imprinting-Like Phenomena in Other Species
The two most important criteria used to identify potential cases of imprinting are: learning by simple exposure, and during a sensitive period. Do other species show filial imprinting similar to that of precocial birds?
Altricial Birds
Several instances of early learning seem to fit these criteria, but similar behaviors do not necessarily mean common mechanisms. In altricial species, the parent-offspring relationship is critical for chick survival. Most species of songbirds are altricial (e.g., sparrows, cardinals, finches). Do these nestlings learn to recognize their parents by simple exposure during a sensitive period?
In altricial chicks, recognition can be assessed in terms of the begging response: Upon arrival of a parent to the nest, nesdings vigorously open their mouths, a response that induces the parent to deliver the food. Experiments with blackbird chicks (Turdus meritin') removed from the nest a few days after hatching and reared in darkness suggest that the development of parent recognition involves exposure learning. Nesdings were exposed to a stuffed model during feeding sessions and later given a preference test between the familiar model and a novel model at ages 10 to 23 days after hatching. Preference for the familiar model was strongest in 11-day-olds, suggesting the presence of a sensitive period (Junco, 1988). Obviously, these nesdings are exposed to instrumental conditioning training (see Box 5.1) since begging (response) is paired with food (reinforcer) in the presence of a parent in the nest (discriminative stimulus). Thus, it is possible that conditioning, rather than exposure, is responsible for the acquisition of a preference for a familiar visual object. However, further experiments suggest that the preference develops even in the absence of food reinforcement. Thus, exposure could be sufficient for acquisition, although food reinforcement would strengthen the filial preference (Junco, 1993).
Migratory Species
Species that exhibit long-range migratory behavior, such as sea turtles and salmon, seem to learn through exposure to the chemical stimuli and magnetic signature characteristic of their early environment (Lohmann, Putman, & Lohmann, 2008). Later, the adult animal uses memory to find a hatching site during breeding. Chemical imprinting and geomagnetic imprinting can be manipulated to repopulate a habitat with an endangered species. For example, eggs of the endangered sea turtle Lepidochelys kempi collected near Rancho Nuevo, Mexico, were placed in containers with sand from Padre Island, Texas (about 400 km north of Rancho Nuevo, on the Gulf of Mexico), to determine whether early exposure could induce the turtles to lay their eggs in Padre Island beaches. Consistent with this hypothesis, 4-month-old turtles spent more time in a compartment labeled with Padre Island sand and sea water
Early Social Learning and Behavior 373 than in a compartment labeled with sand and seawater from Galveston, Texas (approximately 300 km northeast of Padre Island) or in two untreated control compartments (Grassman, Owens, McVey, & Marquez, 1984).
Chemical imprinting also directs the migratory behavior of salmon. Salmon hatch in freshwater streams in the northern continents and then undergo a developmental process known as smoltification—morphological, physiological, and behavioral changes that prepare juveniles as they migrate from freshwater to marine environments. While fish then swim toward the sea, they are exposed to the chemicals in the streams where they hatched—the imprinting migration. Salmon eventually swim upstream of rivers to engage in reproductive behavior—the homing migration. Adults usually die after breeding. Salmon are famous for their tendency to return to the same rivers where they hatched, a behavior suspected to be based on chemical imprinting. Salmon exposed to a water current containing the amino acid L-cysteine during one entire day at various stages during the smoltification phase, and exposed to L-cysteine after smoltification was over, showed a decrease in heart rate typically observed when exposed to familiar stimuli. Such changes peaked for fish exposed to the chemical stimulus between days 21 and 28 of the smoltification phase, but not earlier or later, suggesting a sensitive period (Morin, Dodson, & Doré, 1989).
The brain mechanisms for the imprinting and homing migrations have been described in Pacific salmon (Ueda, 2016). Early exposure to the hatching environment during the imprinting migration triggers the release of hormones from the brain-pituitary-thyroid axis that stimulate the expression of a gene coding for a key component of the NMDA receptor in the basal telencephalon: the NR1 subunit. Expression of the gene coding for the NR1 subunit peaks and then decreases after day 7 of exposure to the hatching environment. This mechanism is thought to trigger the formation of a chemical imprinting memory that will later guide the adult toward the breeding site. Gonadal hormones are involved in the homing migration of the adult salmon into freshwater. Concentrations of the gonadotropin-releasing hormone in the olfactory bulbs peak when salmon are exposed to stimuli from the hatching streams. This is accompanied by enhanced expression of the gene coding for the NR1 subunit of the NMDA receptor in the olfactory bulb, a process thought to be responsible for the retrieval of the imprinting memory established during the imprinting migration.
