Shoaling is a widely important mechanism used by fish in freshwater and marine environments. Although used rather loosely in conjunction with the term “schooling,” the two words differ in definition by nature of organization. Where shoaling refers to a congregation of conspecific fish that stay together, schooling indicates that those fish are swimming in a coordinated fashion. Shoaling is not a learned behavior, but one in which a species is born to participate. This conduct evolved in as many as 50% of all fish species for a number of reasons.
The incentives for shoaling mostly stem from the simple premise that all animals have three jobs in life: eat, reproduce, and avoid being eaten. From this, we can derive the motives for shoaling behavior. To facilitate these life goals, natural selection has chosen for shoaling behavior to increase foraging success, reproductive convenience, hydrodynamic efficiency, social interaction, and predator avoidance (Moyle and Cech 2003, Brahams and Colgan 1985). Fish that engage in shoaling have developed several methods for facilitating the interaction with others.
Individually, shoaling fish have eyes on the sides of their head to better see others in the shoal. Furthermore, it has been demonstrated that vision is important to cohesion because of the inability of most species to maintain schools at night, rather just shoals (Shaw 1961). “Schooling marks” such as prominent stripes or spots help fish recognize others as members of their own species. As a mechanoreceptor, the lateral line system is present in all shoaling fish, assisting in the detection of proximity and movement of other individuals in the shoal.
Aside from physiologically based communication adaptations, chemical communication in the aquatic environment plays a large role in fish interaction. There is ample evidence that chemical composition, concentration, flux, and hydrodynamic transport all have profound effects on chemically mediated ecological processes (Zimmer and Butman 2000). The application of chemical communication in shoaling behavior is vastly important. Most essentially, pheromones serve to aid in association preference of shoal mates, allowing the benefits of shoal behavior to be reaped.
Furthermore, pheromones are pivotal to the advantages of foraging, reproduction, and predator avoidance while in a shoal or school. In this paper, I will describe how pheromones serve to assist shoaling fish in capitalizing on these advantages. Kin and Shoal Mate Association Preferences In order to benefit from the advantages of shoaling, an individual must first associate with a group. Association among fish is often described in terms of cohesion and familiarity. In the case of pheromones, odors are most closely tied to familiarity between fish and chemical recognition of kin.
It is important to understand that in the determination of chemical cues as directors of association preference, visual recognition and chemical recognition are distinguished. Additionally, for some species, chemical cues are more important in shoal cohesion than visual cues. For example, in a study on the effects of diet based cues on shoaling preferences of Threespined Sticklebacks, fish within visual contact of groups of unfamiliar conspecifics showed a significant preference toward the group that had undergone the same diet treatment (p = 0. 001).
This strongly suggests that diet based chemical cues released by Threespined Sticklebacks are a larger consideration than visual cues when selecting shoal association (Ward et al. 2004). Association preference may also be directed by kinship and response to predator stimuli. Association with kin is largely managed by pheromones. In Rainbowfish, Melanotaenia eachamensis, kin recognition is clearly documented and variation in association was significant among different sexes. Males and females both showed a preference to associate with kin of the same sex (p < 0. 05).
However, females preferred to associate with unrelated males (p < 0. 05) (Arnold 2000). Visual cues played an important role here, though olfactory cues likely influence decisions based on hormones and other sexual cues to be discussed later in the paper. Fish may also choose to shoal in the presence of a predator stimuli. When exposed to the chemical stimuli of a predator, the Northern Pike, Fathead minnows (a natural prey) shoal as a predator avoidance mechanism. One experiment tested the level of cohesion between familiar and unfamiliar Fatheads under the condition of the introduced predator stimuli of the
Northern Pike. The study found that Fathead minnows with greater familiarity showed significantly greater cohesion than unfamiliar fish (p = 0. 001). Familiar fish in the experiment had a mean shoaling index of approximately 3. 5, whereas unfamiliar fish had a mean shoaling index of only approximately 2. 75. Familiarity, in this case, was based on the original shoal the Fathead was taken from. Familiar fish were those from the test subject’s original shoal before it was removed. The results of this test indicate that the detection of purely the chemical stimuli leads to a decision on shoal preference.
Moreover, it indicates the preference of the more familiar shoal (Chivers et al. 1995). The preference may also be linked to the similar diet of familiar shoals, as in the case of the Threespined Stickleback, however that postulate has yet to be tested. One unfortunate consequence of industrialism is the introduction of chemical pollutants into the water. One would expect that anthropogenically introduced pollutants would interrupt chemical communication among all fish, not just those that shoal.
In one study, a relevant dose as low as 1µg 1-1 of 4-nonylphenol was sufficient to cause substantial changes in behavior among fish in a shoal. The small dose, regularly recorded in lake around the world, caused Banded Killifish in shoal to avoid the dosed individual. This could lead to significant impacts on the fitness of the individual, providing unnatural selection pressures on populations in affected areas (Ward et al. 2008). Pheromones and Foraging in Shoals One of the most prominent benefits of shoaling behavior is the gained advantage in foraging.
Animals have the ability to determine the type of stimulus by recognizing molecules or combinations of molecules. The unique chemical properties of different foods are therefore detectable by animals. Based on the types of food stimulus present, fish may show a preference for one over another (Zimmer and Butman 2000). Since food preference is clearly directed by chemical cues, it is important to understand how those cues are utilized in a social setting, such as a fish shoal. Finding food is largely a result of olfaction, which in the case of many fish, is associated with pheromones.
Olfaction of a chemical stimulus by one individual of the shoal may lead to that individual directing the shoal toward the stimulus. If the stimulus is a food source, this will benefit the entire shoal. The excitement of one fish into foraging behavior will induce food-searching behavior in others (Pitcher and Parish 1993). In addition, fish in larger schools will find food faster, simply because there are more fish in search (Pitcher et. al 1982). Contrary to the idea that shoaling only helps in locating food, a food source may actually lead to increased shoaling among fish.
According to a study of the influence of diet on shoal cohesion, the odors released from fish on a certain diet will attract conspecifics familiar with that diet. This indicates that chemical cues rooted in the odors of fish preside over the choice in group association (Olsen et al. 2003). While the recognition of chemical cues may be innate, locating food from that cue is sometimes a learned behavior. In this case, shoal membership is beneficial to juveniles learning to forage. Juvenile salmon have demonstrated this ability by repeating the foraging skills they observed for 6 days (Reiriz et al. 998). Given this, it is clear that social learning, as it pertains to foraging techniques, is important and essential to effectively act on food stimuli. Despite the supportive evidence above, there is very little known about the role of pheromones in foraging among fish. One possible role may be in the action of alerting others to the presence of prey, though this has not been tested. Reproduction and Pheromones Sexual reproduction is essential to the existence of fish, and chemical communication has several very important functions that aid in the process.
First, it is central to understand that the advantage of reproduction within a shoal is increased access to potential mates because they are close in proximity. This improves the cost-benefit ratio of searching for a mate and successfully reproducing, respectively. In a shoal, there are a limited number of choices in mate selection. Additionally, since siblings are most likely to associate with the same shoal, there is the potential for inbreeding, resulting in somewhat homogenous offspring. Female Rainbowfish, owever, have demonstrated a preference to associate with unrelated male conspecifics as opposed to male kin. Unfortunately, the function of pheromones in this selection process is somewhat disputed because of the role of visual cues, therefore cannot be confidently stated (Arnold 2000). Although, pheromones can be positively linked to fish migration for spawning purposes, mate selection, courtship, and sex hormones. Pacific Salmon undergo a long range migration from their feeding grounds in the Pacific Ocean to the river in the exact area they were born to reproduce. This process is largely driven by pheromones.
To effectively return to their natal stream, Pacific Salmon must utilize some form of homing mechanism. One study proposes the mechanism is controlled by olfactory imprinting. In this situation, both hatchery-reared and wild salmon showed a tendency to have varying thyroxine levels during different stages of migration (Dittman and Quinn 1996). Thyroxine is a hormone that may be associated with learning. Rapid increases in this hormone level may guide the development of the olfactory system in salmon and help bolster a salmon’s ability to imprint olfactory cues (Nevitt et al. 1994).
In hatchery reared salmon, less erratic changes in thyroxine levels were observed through the course of development. This may be explained by the controlled conditions in the lab and the lack of other influencing stimuli. Nevertheless, peaks in thyroxine levels occurred during hatching/emergence, rapid growth, and hatchery release. The only peak to surpass the imprinting threshold occurred during hatchery release, suggesting the importance of this stage in development to learning homing cues. The instance of the wild salmon is slightly more complex because of the influence of changing environmental stimuli.
Despite this, wild salmon indicated a thyroxine level above imprinting threshold once just after emergence, once following rapid growth, and once during parr-smolt transformation (which is analogous to hatchery release in hatchery salmon). The former two peaks were brief, spending less than a month above the threshold, while the latter, during parr-smolt transformation, remained above imprinting level for approximately two and a half months. This data yields the same conclusion as in hatchery-reared salmon, that parr-smolt transformation must be important to olfactory imprinting.
The other peaks are evidence that wild salmon not only imprint stimuli at predetermined intervals of development, but at times during the migration when it might be most beneficial (Dittman and Quinn 1996). This study supports the notion that homing in pacific salmon, especially during the freshwater phase of migration, is largely driven by olfactory stimuli present in the environment. Because those stimuli are unique to each headwater stream, Pacific salmon can successfully return to their natal location to spawn. Homing is not the only aid to successful sexual reproduction where pheromones are of consequence.
Within mate selection and courtship, chemicals released by males and females have been found to elicit a response of conspecifics of the opposite sex. In a lab setting, mature male Sea Lampreys have been shown to release a signal pheromone, attracting females for reproduction. The chemical 3-Keto-petromyzonol-sulphate (3K-PS) not only strongly attracted ovulated females over non ovulated females, but stimulated searching for a mate (Stacey and Sorensen 2005). Pheromones for example, in the post-ovulatory female Rainbow Trout, Salmo gairdneri, release a pheromone affecting the behavior of male Rainbow Trout.
When placed in the presence of pre-ovulatory eggs and post-ovulatory ovaries of the female, male Rainbow Trout tended to be attracted to the post-ovulatory ovaries, indicating a clear discrimination between the two. Furthermore, the presence of post-ovulatory ovaries educed courtship behavior of males. It was concluded that the function of pheromones in Rainbow Trout was to inform males of the ovulation of females, attract males, and elicit courtship behavior of the males. Clearly, chemical cues play a heightened role in the reproductive process of Rainbow Trout (Honda 1980).
Since the publication of the above article on Rainbow Trout, further investigation into hormonal pheromones and their function in fish have been done. It is now understood that most pheromones used in reproduction among fish are derived from steroid and prostaglandin hormones. Through evolution, adaptive radiation, and fish speciation, different species have developed diverse forms of these hormones, method of detection, and uses for each. Moreover, these varying hormones are species specific and elicit unique responses for each species (Sorensen and Stacey 1998).
Predator Avoidance One of the most well known advantages of shoaling in fish is schooling as a predator avoidance mechanism. Shoaling helps the individual fitness of an organism by creating two effects. The first is the confusion effect and is based on the idea that it becomes difficult for a predator to select an individual when it is part of a large school (Milinski and Heller 1978). To illustrate, when fish all look the same, are the same size, and shiny, a predator will have difficulty maintaining a single strike target.
The second effect is the many eyes effect. This is based on the fact that with more individuals searching, there is a higher likelihood that a predator be detected before attacking (Roberts 1996). This is advantageous because early detection of danger allows the shoal more time to avoid predation. Early detection of predators as an avoidance mechanism utilized by shoaling fish is closely linked to chemical communication (Lima and Dill 1990). A popular theory of the role of chemical cues in this application is alarm pheromones.
In fish, it is speculated that a strong chemical signal is released in the presence of as predator, which functions to alert others within the shoal of impending danger. This has been demonstrated in a number of cases. Brown et al. 2001, in a study on Fathead minnows and predator detection, successfully showed that the minnows could learn to recognize predator odors (commonly associated with pheromones), even at levels below their alarm threshold. To clarify, many fish that use alarm cues have a stimulation threshold, beyond which they initiate a response.
If the concentration of a chemical stimulus is below this threshold, fish will be aware of the presence, but not alarmed until stronger cues are received (Brown et al. 2001). The Fathead minnow’s ability to detect predator pheromones prior to imminent danger will serve to improve their fitness. The Fathead minnow’s ability to learn to detect predator cues may be an evolutionary adaptation used by all shoaling fish. This may have an important implication in shoaling fish, as social learning has been documented (Lachlan et al. 1998).
The presence of an alarm pheromone in certain species of shoaling fish, as demonstrated in a lab, has been confirmed in a wild setting (Wisenden et al. 2004). Many taxa of fish contain chemical cues within their skin which may only be released when tissue is damaged. Laboratory tests indicated antipredator behavioral responses when exposed to these cues, however field observation in a wild setting observed a lack of response in many cases. Following this discovery, an experiment mimicking the lab experiment confirming a response was conducted in the wild.
The study focused on Blacknose Shiners, Notropis heterolepis, and Glowlight Tetras, Hemigrammus erythrozonus, where the goal was to determine their response to predator chemical cues. In the case of the shiners, they observed a decrease in the number of fish present in areas where the predator chemical cue was also present. For the tetras, the researchers noted that the visual cue of a predator was significantly increased after receiving a chemical predator cue. They concluded that chemical cues result in three modes of response.
The pheromone served to inform the prey of impending risk, induces predator avoidance behavior, and affects the intensity of the behavioral response elicited by other sensory modes such as visual cues. Furthermore, the behavioral response to an alarm pheromone is largely context dependent, as evident by the difference in response levels between fish in a lab and fish in the wild (Wisenden et al. 2004). Alarm pheromones released by damaged tissue may also have a secondary benefit. While they are most commonly understood to be used in warning other conspecifics, after the attack of prey they may also serve to help ward off predators indirectly.
The cues released by captured prey have been shown to not only alert other prey of danger, but also attract secondary predators (Mathis et al. 1995). In a study on Ostariophysan fishes, commonly understood to contain an alarm pheromone in the skin, the benefit of attracting secondary predators was observed. Fathead Minnows demonstrated a higher probability of escaping predation when predation is interrupted by a secondary predator. In this study, in the presence of a secondary predator, five of thirteen shoals were able to escape predation.
No shoals escaped predation in the absence of a secondary predator. This research supports the position that chemical cues may have an indirect benefit to predator avoidance (Chivers et al 1996). Shoal cohesion is also affected by the presence of chemical alarm cues. In the absence of a shoal, a fish exposed to a predator pheromone will seek to avoid the area where that cue is detected. However, in the presence of a shoal and a chemical cue, an alarmed individual will join the shoal, even if the shoal is still in the presence of an alarm pheromone (Wisenden et al. 2003).
This can partly be explained by the idea that the probability of an individual getting eaten is reduced when there are more prey present (Krause et al. 1998). Summary and Conclusions The role of animals in an aquatic system is based on a simple premise that an individual, in its lifetime, must eat, reproduce, and avoid predation. One of the most popular ways fish have evolved to accomplish these goals is to participate in shoaling for some or all of their life. The shoaling facilitates foraging, eases the process of reproduction, and aids in predator avoidance mechanisms.
The objective of this paper is to expose the role of pheromones in facilitating the experience of these benefits. Additionally, pheromones serve to aid in association preference of shoal mates. This is important because a cohesive shoal can benefit most effectively. When forming a shoal, an important consideration for fish is which fish to associate with. Several experiments have evaluated this and research has provided evidence that chemical cues participate in the process. Threespined Sticklebacks, when given a choice, show a high preference toward shoals that had undergone similar diet treatments as the focal fish.
This strongly indicates the likelihood of some pheromone, released by the shoaling fish, associated with diet. Additionally, familiarity is important to shoal cohesion, especially under the risk of predation. Under a predator stimulus, Fathead minnows favored familiar shoals over unfamiliar ones. It is also important to understand the relationship of humans to chemical communication and shoal cohesion. An unfortunate circumstance of a growing society is pollution of local waterways. When introduced to Banded Killifish, small doses of pollutant lowered cohesion and actually caused the shoal to avoid the infected individual.
This will have a profound effect on the fitness of infected individuals because they will not be able to procreate if all potential mates avoid them. Pheromones also act in aiding the process of foraging in shoals. Most of predation in the aquatic environment is regulated by olfaction and recognition of a food stimulus. When a fish recognizes a food source and begins eating, others in the shoal will be excited into searching for food. Because social learning had been documented in shoals, the process of foraging based on recognition of chemical food cues is facilitated for juveniles.
It is also important to note that shoal cohesion can also be influenced by diet based chemical cues released by fish. Fish are attracted to conspecifics based on the familiarity of these recognized diet cues. Arguably the most important consideration to the survival of a species is reproduction. Again, pheromones help direct many processes associated with reproduction. In migratory species such as the Pacific Salmon, the environmental chemical stimuli are responsible for homing. It is commonly known that Pacific Salmon return to their natal stream to spawn when they are sexually mature.
Returning to the exact location would be difficult without some form of imprinting in their memory. It is posited that environmental stimuli acting on juvenile Pacific Salmon raise levels of the hormone thyroxine above the imprinting threshold during pre-determined times during their development. This is strong evidence to support the idea that Salmon pheromones, in conjunction with environmental stimuli, are responsible for making homing possible. Courtship and mating are also a high consideration when discussing the role of pheromones. In sea lampreys, the sexually mature males release a chemical to attract female mates.
Conversely, female Rainbow Trout excrete a pheromone after ovulation, drawing sexually mature male Rainbow Trout. While hormonal differences among species of fish are easily observed now, they were not always so varied. In fact, most hormones used in fish are derived from steroids or prostaglandins. Through the evolution of species, the base hormones evolved as well. Now, most species have their own unique hormones, their own unique detection mechanisms, and their own unique responses. Finally, and quite possibly they strongest argument for shoaling, is the mechanism of predator avoidance.
As pheromones relate, they are most closely tied to alarm signals. Predators often provide chemical cues, alerting prey to their presence. Recognizing these signals is easily learned in shoals due to the social interaction of the fish. Alarm pheromones are present in the tissue of most fish and released when the tissue is damaged. The reaction to these pheromones had been demonstrated in the wild using shiners and tetras. It is conceived that the detection of an alarm pheromone serves to inform others of the presence of a predator, induce avoidance behavior, and intensify the response to visual cues.
It is vital to understand that the reaction to alarm cues is largely context depended, as indicated in a lower response to cues in a natural environment than in a lab setting. Alarm cues may have other benefits as well. In some instances, release of alarm cues may attract secondary predator, interrupting predation and increasing the probability of evasion. Predator cues have also been shown to improve fish cohesion, which can be explained by the idiom, “safety in numbers. ” Fish tend to join shoals in the presence of predator stimuli, thereby lowering their probability of getting eaten.
In conclusion, there are several important considerations to be made when reviewing the role of pheromones in shoaling behavior. First, much of the benefits of pheromonal communication are spatially dependent. Shoals may provide a more effective medium of communication because they are close in proximity. In an aquatic environment, dispersal and dilution of chemical signals is high, therefore organisms in close proximity are most likely to receive cues and react in sufficient time. Secondly and most importantly, responses of organisms are usually directed by pheromones in conjunction with other cues.
As shown in the case of the Glowlight Tetra, the response to visual cues is intensified after receiving a chemical cue. Based on the aggregation of the reports above, there is clear evidence that pheromones do, however play a pivotal role in the function of the benefits reaped by shoaling behavior.
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