In 1938, the Austrian ethologist Karl von Frisch made his first report on the existence of the chemical alarm signal known as Schreckstoff (fright substance) in minnows. An alarm signal is a response produced by an individual, the "sender", reacting to a hazard that warns other animals, the receivers, of danger. [1] This chemical alarm signal is released only when the sender incurs mechanical damage, such as when it has been caught by a predator, and is detected by the olfactory system. When this signal reaches the receivers, they perceive a greater predation risk and exhibit an antipredator response. Since populations of fish exhibiting this trait survive more successfully, the trait is maintained via natural selection. While the evolution of this signal was once a topic of great debate, recent evidence suggests schreckstoff evolved as a defense against environmental stressors such as pathogens, parasites, and UVB radiation and that it was later co-opted by predators and prey as a chemical signal.
Chemical alarm systems have been identified in a number of different taxa, including gastropods, [2] echinoderms, [3] amphibians [4] and fishes. One of the most well-studied chemical alarm signals is schreckstoff, the use of which is widespread in the superorder Ostariophysi (e.g., minnows, characins, catfishes, etc.). About 64% of all freshwater fish species and 27% of all fish species worldwide are found in the ostariophysan superorder, which highlights the widespread use and importance of this chemical alarm system in fishes. [5]
The production of schreckstoff has been shown to be metabolically expensive and is therefore part of a conditional strategy that can only be employed by individuals with access to sufficient resources. [6] One putative active ingredient in schreckstoff is hypoxanthine-3N-oxide (H3NO), which may be produced in club cells which will henceforth be referred to as "alarm substance cells". [7] The nitrogen oxide functional group was found to be the main chemical trigger of antipredator behavior in receivers. [8] Schreckstoff is a mixture, and fragments of a glycosaminoglycan, chondroitin sulfate, are able to trigger fear responses. [9] The precursor polysaccharide is a component of mucus, and fragments are proposed to be produced during injury. Like schreckstoff obtained from skin extract, chondroitin sulfate activates a subset of olfactory sensory neurons.
Production of and responses to schreckstoff change over the course of ontogeny. For example, young brook sticklebacks (Culaea inconstans) are more likely to be caught in minnow traps that have been baited with conspecific skin extracts than adults. [10] This result indicates young brook sticklebacks do not make the association between schreckstoff and the potential presence of a predator as readily as adults. Whether this association strengthens over time as a result of learning or physiological development remains unclear. [11]
In addition to changes across ontogeny, the degree to which schreckstoff is produced varies within the breeding season. Male fathead minnows (Pimephales promelas) cease production of schreckstoff during the breeding season, but still exhibit antipredator behaviors in response to schreckstoff during this time. [12] Schreckstoff production may be halted at this time because male fathead minnows often incur mechanical damage while building their nests. It would be detrimental to a male to produce schreckstoff while building a nest, as it would inadvertently repel females, thereby decreasing the likelihood of obtaining a mate. By ceasing schreckstoff production during the breeding season, males circumvent this problem. The cessation of alarm substance cell production appears to be controlled by androgens. [13]
A number of different hypotheses have been proposed for the evolution of schreckstoff. [14] The first hypothesis is that the evolution of schreckstoff has been driven by kin selection. Support for this hypothesis would include evidence that individuals live in groups of closely related kin and that the release of chemical alarm signals increases the likelihood that related individuals will avoid predation. The second hypothesis, predator attraction, suggests the release of schreckstoff may attract additional predators which will interfere with the predation event, increasing the likelihood that the prey will escape and survive the attack. This hypothesis assumes predators will be attracted to schreckstoff and will interfere with one another either through competition for the captured prey or through predation of one another. It additionally assumes, despite the fact that the prey has already incurred mechanical damage, it is possible for the prey to escape and recover from the attack. Testing and validating these assumptions would provide support for the predator attraction hypothesis. The third hypothesis proposes that schreckstoff has an immune function, providing protection against pathogens, parasites and/or UVB radiation. For this hypothesis to be supported, a correlation between alarm substance cell production and the presence of pathogens and parasites would need to be observed. Direct evidence that schreckstoff inhibits the growth of aquatic pathogens and parasites would provide additional support for the immunity hypothesis. Another hypothesis is that schreckstoff is a breakdown product of mucus and club cells, induced by injury. Selection for the alarm response is primarily at the level of the receiver.
One of the first hypotheses for the evolution of schreckstoff centered on W.D. Hamilton’s theory of kin selection. [15] Under the theory of kin selection, the sender of the chemical alarm signal would be willing to incur the costs of sending this signal if the benefits to related individuals were sufficiently high. In a situation where the sender of the signal is paying great costs (i.e., it releases the chemical alarm signal because it has incurred potentially mortal mechanical damage), the benefits to closely related kin would have to be great. Under the framework of kin selection, behaviors that are seemingly detrimental to the sender are selected because they benefit individuals that are likely to share alleles by common descent. In this way, the frequency of the sender's alleles in the next generation is increased by their presence in successful kin.
To apply kin selection theory to the evolution of schreckstoff, a number of conditions must be met. First, evidence must exist for the release of schreckstoff by the sender confers benefiting the receivers. Second, it must be shown that individuals in the order Ostariophysi associate mainly with family members. If either of these two assumptions is violated, then the kin selection hypothesis would not be supported.
Some evidence exists in support of the first assumption that the release of schreckstoff confers quantifiable advantages to the receivers of this chemical signal. A laboratory experiment [16] revealed that fathead minnows exposed to conspecific schreckstoff survived 39.5% longer than controls when placed in a tank with a predatory northern pike (Esox lucius). This finding suggests schreckstoff increases vigilance in receivers, resulting in a quicker reaction time following detection of the predator.
The second assumption, that individuals in the order Ostariophysi associate with close family members, does not appear to be supported by empirical evidence. In shoals of European minnows (Phoxinus phoxinus), no difference in relatedness was found within and between shoals, [17] indicating individuals are not associating more closely with relatives than nonrelatives. Shoal composition has not been examined in all members of the ostariophysan order, and shoals composed entirely of family members may yet be discovered. Nevertheless, the finding that schreckstoff production is maintained in a species where the function is clearly unrelated to kin benefits provides strong evidence against kin selection as a mechanism for the evolution of schreckstoff.
Fathead minnows have also been found to produce fewer epidermal alarm substance cells (and therefore less schreckstoff) when in the presence of familiar shoalmates. [18] The results of this study indicate one of two scenarios, neither of which is compatible with the hypothesis that schreckstoff evolved by kin selection. First, if schreckstoff evolved by kin selection, more epidermal alarm substance cells would be expected to be produced in the presence of kin than nonkin. This means familiar shoalmates in fathead minnows should be closely related kin and schreckstoff production should be increased when in shoals with familiar individuals. The study did not find this to be the case. [19] Second, these results indicate individuals either do not associate with kin at all or production of schreckstoff varies depending on how familiar the focal fish is with the individuals with which it shoals. In conclusion, evidence does not support the hypothesis that schreckstoff evolved because it bolstered the inclusive fitness of the sender through increased survival of kin.
The predator attractant hypothesis proposes that the main purpose of schreckstoff is to attract additional predators to the area. [20] According to this hypothesis, additional predators will interact with the initial predator, and these interactions will provide the sender with an opportunity to escape. A number of conditions must be met to support this hypothesis. First, schreckstoff must attract predators. Second, subsequent predators must disrupt the predation event, thereby increasing the probability that the prey will escape. Third, the sender must be able to recover from the mechanical damage incurred during the predation event.
A study [21] provides support for the first condition that the release of schreckstoff must attract predators. This experiment revealed that schreckstoff extracted from the skin of fathead minnows attracted both northern pike (Esox lucius) and predatory diving beetles (Colymbetes sculptilis). Additionally, a natural study showed that predatory fish were seven times more likely to strike a lure baited with a sponge soaked in fathead minnow skin extract than a sponge soaked in either water or skin extract from a nonostariophysan convict cichlid (which presumably does not produce schreckstoff). [22]
While the previous two studies provided examples of systems in which schreckstoff acts to attract additional predators, a system was found for which this was not the case. [23] Spotted bass (Micropterus punctulatus) were exposed to skin (containing schreckstoff) and muscle (control, containing no schreckstoff) extracts from five different co-occurring prey species. The spotted bass were not attracted to any of the schreckstoff treatments. This result indicates schreckstoff does not always attract relevant predators in the area. Northern pike are an introduced species in many areas, so were not likely to be coevolving with fathead minnows during the evolution of the schreckstoff system. This system may be more ecologically relevant and little evidence suggests schreckstoff evolved as a predator attractant. In conclusion, the debate continues over whether or not the first condition for this hypothesis has been met.
The second condition that needs to be met in support of the predator attraction hypothesis is that additional predators must occasionally disrupt predation events, increasing the probability that prey will escape. In the northern pike/fathead minnow system, additional northern pike may interfere with a predation event in one of two ways. [24] First, additional northern pike of the same size interfere with a predation event by coming into contact with the main predator (biting it, etc.). Second, additional pike of larger size attracted to schreckstoff may prey on the initial predator.
The probability that fathead minnows escape after being captured by a northern pike significantly increases when a second pike interferes with the predation event. [25] The northern pike have an age-structured population biased towards younger, smaller individuals. If a younger pike attacks a fathead minnow and attracts an older, larger conspecific, then the younger pike may be at risk of cannibalism and will be inclined to release the prey to focus on escape. In regards to the second condition, additional predators do appear to disrupt predation events, increasing the probability that the sender will escape. The final condition, that individuals need to successfully recover from a predation event, appears to be satisfied. Support for this condition comes from the observation that many small fishes in natural populations exhibit scars, presumably from failed predator attempts. [26]
While the evidence that schreckstoff attracts predators is mixed, studies indicate multiple predators will interfere with each other and prey can recover from predation events when they manage to escape. The extent to which predators are attracted to a predation event depends upon the speed at which schreckstoff diffuses through its aquatic environment, which in turn depends upon water flow parameters. This hypothesis indicates schreckstoff evolved as a way of increasing the probability of survival during a predation event and its role as a predator cue for conspecifics evolved subsequently. Supported by more empirical studies than the kin selection hypothesis, the predator attraction hypothesis remained popular for quite some time.
The final hypothesis posits that schreckstoff has an immune function and may be the first line of defense against pathogens, parasites, and/or UVB radiation. Evidence for this hypothesis is strong. A recent comprehensive study [27] revealed that exposure to parasites and pathogens that penetrate the skin of ostariophysans stimulated the production of alarm cells. Additionally, increased exposure to UV radiation was correlated with an increase in alarm cell production.
The role of schreckstoff in immune response was further strengthened by the finding that skin extracts from fathead minnows inhibited the growth of Saprolegnia ferax (a water mould) in culture. In contrast, skin extracts from swordtails ( Xiphophorus helleri), which are not believed to produce schreckstoff, increased S. ferax growth compared to controls. Cadmium, a heavy metal and an immunosuppressant in vertebrates, [28] inhibits the production of alarm cells when fishes are infected with Saprolegnia. [29] Furthermore, a follow-up study [30] treated fathead minnows with cortisol, a well-known immunosuppressant, which significantly reduced alarm cell investment in conjunction with leukocyte activity. The results of these extensive studies strongly suggest schreckstoff's main function is to provide immunity against a number of environmental threats aimed at the fish's epidermis.
If schreckstoff evolved as a defense against pathogens, parasites, and UVB radiation, then the release of schreckstoff into the environment subsequently allowed for both predators and prey to exploit this system. Predators in some systems may use schreckstoff as a cue for an easy meal, either by disrupting the predation event to steal the prey item for themselves or by preying on the initial predator. Nearby conspecifics then exploit schreckstoff as a chemical cue, alerting them to the presence of a predator in the area.
The most convincing research to date indicates alarm substance cells serve as an immune system response and the ecological ramifications of this substance as a chemical alarm signal developed subsequently. This finding generates a number of interesting research questions. First, as mentioned earlier, males in many ostariophysan species cease production of alarm substance cells during the breeding season, presumably so females are not inadvertently repelled from the nest when males incur mechanical damage during nest building. In light of the immune hypothesis, alarm substance cells possibly are instead produced less during the breeding season because increased testosterone levels may decrease immune responses. [31] Additionally, this finding indicates males are at a greater risk from UVB radiation, as well as parasite and pathogen infection, during the breeding season.
The role of schreckstoff as an immune response has additional implications in this age of increasing environmental change. [32] Environmental stressors, including UVB radiation, pollution, and parasites, are increasing in the environment, and are likely to continue increasing over time. UVB radiation exposure is increasing due to decreases in stratospheric ozone, [33] diseases are becoming increasingly important at both local and global scales, [34] and pollutants, including heavy metals, are being introduced into ecosystems. [35] If cadmium, the heavy metal affecting the fish's ability to produce schreckstoff in response to environmental stressors, increased in concentration in the environment, the immune response of many ostariophysan fishes would be compromised. [36]
Predation is a biological interaction where one organism, the predator, kills and eats another organism, its prey. It is one of a family of common feeding behaviours that includes parasitism and micropredation and parasitoidism. It is distinct from scavenging on dead prey, though many predators also scavenge; it overlaps with herbivory, as seed predators and destructive frugivores are predators.
Animal communication is the transfer of information from one or a group of animals to one or more other animals that affects the current or future behavior of the receivers. Information may be sent intentionally, as in a courtship display, or unintentionally, as in the transfer of scent from predator to prey with kairomones. Information may be transferred to an "audience" of several receivers. Animal communication is a rapidly growing area of study in disciplines including animal behavior, sociology, neurology and animal cognition. Many aspects of animal behavior, such as symbolic name use, emotional expression, learning and sexual behavior, are being understood in new ways.
The Eurasian minnow, minnow, or common minnow is a small species of freshwater fish in the carp family Cyprinidae. It is the type species of genus Phoxinus. It is ubiquitous throughout much of Eurasia, from Britain and Spain to eastern Siberia, predominantly in cool streams and well-oxygenated lakes and ponds. It is noted for being a gregarious species, shoaling in large numbers.
Anti-predator adaptations are mechanisms developed through evolution that assist prey organisms in their constant struggle against predators. Throughout the animal kingdom, adaptations have evolved for every stage of this struggle, namely by avoiding detection, warding off attack, fighting back, or escaping when caught.
In animal communication, an alarm signal is an antipredator adaptation in the form of signals emitted by social animals in response to danger. Many primates and birds have elaborate alarm calls for warning conspecifics of approaching predators. For example, the alarm call of the blackbird is a familiar sound in many gardens. Other animals, like fish and insects, may use non-auditory signals, such as chemical messages. Visual signs such as the white tail flashes of many deer have been suggested as alarm signals; they are less likely to be received by conspecifics, so have tended to be treated as a signal to the predator instead.
The rough-skinned newt or roughskin newt is a North American newt known for the strong toxin exuded from its skin.
The golden shiner is a cyprinid fish native to eastern North America. It is the sole member of its genus. Much used as a bait fish, it is probably the most widely pond-cultured fish in the United States. It can be found in Quebec, and its French name is "Mené jaune" or "Chatte de l'Est".
Interspecies communication is communication between different species of animals, plants, or microorganisms.
Cannibalism is the act of consuming another individual of the same species as food. Cannibalism is a common ecological interaction in the animal kingdom and has been recorded in more than 1,500 species. Human cannibalism is well documented, both in ancient and in recent times.
Fathead minnow, also known as fathead or tuffy, is a species of temperate freshwater fish belonging to the genus Pimephales of the cyprinid family. The natural geographic range extends throughout much of North America, from central Canada south along the Rockies to Texas, and east to Virginia and the Northeastern United States. This minnow has also been introduced to many other areas via bait bucket releases. Its golden, or xanthic, strain, known as the rosy-red minnow, is a very common feeder fish sold in the United States and Canada. This fish is best known for producing Schreckstoff.
Pomphorhynchus laevis is an endo-parasitic acanthocephalan worm, with a complex life cycle, that can modify the behaviour of its intermediate host, the freshwater amphipod Gammarus pulex. P. laevis does not contain a digestive tract and relies on the nutrients provided by its host species. In the fish host this can lead to the accumulation of lead in P. laevis by feeding on the bile of the host species.
An eyespot is an eye-like marking. They are found in butterflies, reptiles, cats, birds and fish.
Mobbing in animals is an antipredator adaptation in which individuals of prey species mob a predator by cooperatively attacking or harassing it, usually to protect their offspring. A simple definition of mobbing is an assemblage of individuals around a potentially dangerous predator. This is most frequently seen in birds, though it is also known to occur in many other animals such as the meerkat and some bovines. While mobbing has evolved independently in many species, it only tends to be present in those whose young are frequently preyed upon. This behavior may complement cryptic adaptations in the offspring themselves, such as camouflage and hiding. Mobbing calls may be used to summon nearby individuals to cooperate in the attack.
Pseudochromis fuscus is a species of saltwater fish in the dottyback family. Dottybacks are generally very bright in color and relatively small, factors which have made them popular among aquarium enthusiasts. Besides their coloration and size, they are probably best known for their aggressive temperament. While many of the more common dottybacks are in the Pseudochromis genus, there are also species in other genera. Common names for this particular species include the brown dottyback, the golden dottyback, and the musky dottyback. The common name “Golden dottyback” is shared with another species of dottyback, the Pseudochromis pseudoplesiopinae. The species name, fuscus, means dark or dusky in Latin.
In biology, any group of fish that stay together for social reasons are shoaling, and if the group is swimming in the same direction in a coordinated manner, they are schooling. In common usage, the terms are sometimes used rather loosely. About one quarter of fish species shoal all their lives, and about one half shoal for part of their lives.
Chemical defense is a strategy employed by many organisms to avoid consumption by producing toxic or repellent metabolites or chemical warnings which incite defensive behavioral changes. The production of defensive chemicals occurs in plants, fungi, and bacteria, as well as invertebrate and vertebrate animals. The class of chemicals produced by organisms that are considered defensive may be considered in a strict sense to only apply to those aiding an organism in escaping herbivory or predation. However, the distinction between types of chemical interaction is subjective and defensive chemicals may also be considered to protect against reduced fitness by pests, parasites, and competitors. Repellent rather than toxic metabolites are allomones, a sub category signaling metabolites known as semiochemicals. Many chemicals used for defensive purposes are secondary metabolites derived from primary metabolites which serve a physiological purpose in the organism. Secondary metabolites produced by plants are consumed and sequestered by a variety of arthropods and, in turn, toxins found in some amphibians, snakes, and even birds can be traced back to arthropod prey. There are a variety of special cases for considering mammalian antipredatory adaptations as chemical defenses as well.
Insects have a wide variety of predators, including birds, reptiles, amphibians, mammals, carnivorous plants, and other arthropods. The great majority (80–99.99%) of individuals born do not survive to reproductive age, with perhaps 50% of this mortality rate attributed to predation. In order to deal with this ongoing escapist battle, insects have evolved a wide range of defense mechanisms. The only restraint on these adaptations is that their cost, in terms of time and energy, does not exceed the benefit that they provide to the organism. The further that a feature tips the balance towards beneficial, the more likely that selection will act upon the trait, passing it down to further generations. The opposite also holds true; defenses that are too costly will have a little chance of being passed down. Examples of defenses that have withstood the test of time include hiding, escape by flight or running, and firmly holding ground to fight as well as producing chemicals and social structures that help prevent predation.
Pursuit predation is a form of predation in which predators actively give chase to their prey, either solitarily or as a group. It is an alternate predation strategy to ambush predation — pursuit predators rely on superior speed, endurance and/or teamwork to seize the prey, while ambush predators use concealment, luring, exploiting of surroundings and the element of surprise to capture the prey. While the two patterns of predation are not mutually exclusive, morphological differences in an organism's body plan can create an evolutionary bias favoring either type of predation.
The predation risk allocation hypothesis attempts to explain how and why animals' behaviour and foraging strategies differ in various predatory situations, depending on their risk of endangerment. The hypothesis suggests that an animal's alertness and attention, along with its willingness to hunt for food, will change depending on the risk factors within that animal's environment and the presence of predators that could attack. The model assumes there are different levels of risk factors within various environments and prey animals will behave more cautiously when they are found in high-risk environments. The overall effectiveness of the model for predicting animal behaviour varies, therefore, its results are dependent on the prey species used in the model and how their behaviour changes. There are several reasons the predation risk allocation hypothesis was developed to observe how animal behaviour varies depending on its risk factors. Mixed results have been found for the model's effectiveness in predicting predator defensive behaviour for various species.
Egg predation is a feeding strategy in many groups of animals (ovivores) in which they consume eggs. Since an egg represents a complete organism at one stage of its life cycle, eating an egg is a form of predation, the killing of another organism for food.