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Chapter 2 Definitions of Types of Symbioses
CHAPTER 2
DEFINITIONS OF TYPES OF SYMBIOSES I n studying heterospecific associations among organisms, a number of terms have been coined to describe types of relationships. These, however, like so many biological terms, are essentially operational words that are defineable only within broad limits. They are nevertheless useful in that they permit the filing of data into convenient, although in some instances poorly defined and overlapping, compartments. Specifically, the terms symbiosis, parasitism, commensalism, mutualism, inquilinism, phoresis and even predation are often found in the literature pertaining to heterospecific associations. In recent years, various authors (including Lapage, 1958 ; Baer, 1952; Caullery, 1952; Cameron, 1956; Dales, 1957, 1966; Hopkins, 1957b; Yonge, 1957; Dogiel, 1962; Olsen, 1962; Noble and Noble, 1961; Smyth, 1962 ; Sprent, 1963 ; Lincicome, 1963; Cheng, 1964b ; Geiman, 1964; Henry, 1966; Croll, 1966) have presented and discussed definitions for terms that describe heterospecific associations, and, as to be expected, differences, depending upon the immediate interests of the author, exist, sometimes only slightly. I n order that the meanings implied by me in the subsequent pages are clear, those terms that I consider useful are defined below.
I. SYMBIOSIS The term symbiosis, as originally coined by De Bary (1879) to mean no more than " living together ", is being retained in its original sense, although some authors have used symbiosis as a synonym of mutualism. Thus symbiosis is the broad, all-encompassingterm used to describe all types of heterospecific associations, excluding predation, during which there exists physical contact or intimate proximity between the two members. There are no implications of benefit acquirement or giving, nutritional dependency, or infliction or receipt of harm. Thus symbiosis is a broad ecological term under which can be categorized parasitism, commensalism, mutualism and phoresis. AS explained later, I have chosen to consider inquilinism to be no different from commensalism. It is with this or a very'similar definition in mind that Read (1958a) has suggested " a science of symbiosis " and Noble 4
2. DEFINITIONS OF TYPES OF SYMBIOSES
5
and Noble (1961) have expressed the view that because of the modern trends in parasitology, parasitologists might be designated as “ symbiontologists ”. I, however, prefer the term symbiology (Cheng, 196410) over “ symbiontology ”, since the latter implies that the investigator and his discipline are only concerned with one member of the association, the symbiont, and not with the host. As stated earlier, if the study of relationships between heterospecific organisms is to be comprehensive and unique, both the host and the symbiont, plus the nature of the relationship, must be taken into consideration. As stated, several subcategories of symbioses have long been in use in the biological literature. These are redefined below, and are drawn from what are considered to be the most appropriate aspects of previous definitions, although the basic interpretations are those of Smyth (1962).
A. Parasitism Parasitism describes a heterospecific relationship, be it permanent or temporary, during which there exists metabolic dependence of the parasite, the smaller of the two species, on its host. This metabolic dependency may be in the form of nutritional materials, digestive enzymes, developmental stimuli, or control of maturation. With the acceptance of this definition, Smyth (1962) has pointed out that it is now possible “ t o draw up a list of parasitic species which show an increasing degree of metabolic dependence on their hosts ”. Along this hypothetical scale (Fig. l), one can assign free-living organisms to one METABOLICDEPENDENCE Free-living
1
0%
1 Totally parasitic
100%
FIG.1. Diagram showing the relative concept of parasitism based on the degree of metabolic dependence. (After Smyth, 1962.)
terminal and complete dependence, or total parasitism, to the other. It should be pointed out, however, that if the parasite is metabolically dependent on the host even for a single factor, which cannot be obtained from the microenvironment, the relationship becomes an obligatory one if the parasite is to survive and perpetuate its species. Thus “ total dependence ” describes the number of metabolic factors on which the parasite is dependent and not necessarily the extreme at one end of a gradient of relationships.
6
MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES
B. Mutualism Mutualism describes an intimate relationship during which both the mutualist and the host are metabolically dependent on each other. An often cited example of mutualism is that relationship between the cnidarian Chlorohydra viridissima and the green alga Zoochlorella, which lives in the cytoplasm of the nutritive-muscular cells of the cnidarian’s gastrodermis. The alga produces oxygen which Chlorohydra utilizes, and Zoochlorella makes use of the nitrogenous waste products of Chlorohydra for its synthetic processes. Thus there exists interdependency between the mutualist and host. I n addition to this aspect of metabolic dependency, others exist (Muscatine and Lenhoff, 1965a,b ; Muscatine, 1965). What appears to be a concise distinction between parasitism and mutualism has been partially shattered by Smyth’s (1962) viewpoint that mutualism is actually a specialized form of parasitism during which some metabolic by-products of the parasite are of value to the host. Nevertheless, the mutual dependency is a real, recognizable and obligatory one during mutualistic, but not during parasitic, relationships.
C. Commensalism Commensalism describes that type of more or less intimate relationship during which the commensal generally derives physical shelter from the host, is nourished on foods that are associated but not a part of the host, and is not metabolically dependent on the host. Literally, commensalism means “ eating at the same table ”. It is thus a loose type of relationship and is not an obligatory one. I n accepting this definition, there is no longer a need to have a special category of inquilinism as defined by Caullery (1952). One of the best known examples of commensalism is found within the realms of marine biology. This is the association between certain species of hermit crabs and sea anemones. The anemone lives on the shell sheltering the hermit crab, At this location, it benefits directly in that it has access to the food caught and scattered by the crab. I n return, the crab benefits from the presence of the anemone which aids in warding off predators. Yet each animal can live without the other. Not all anemone-hermit crab associations are commensalistic. For example, Faurot (1910) has shown that the relationship between the hermit crab Eupagurus prideauxi and the anemone Adamsia palliata is an obligatory one, since neither of the partners will survive alone. Here the relationship appears to have developed into a mutualistic one.
2. DEFINITIONS O F TYPES O F SYMBIOSES
7
D. Phoresis Phoresis is most akin to commensalism but does not involve “ eating at the same table ”. This type of relationship is again a loose and nonobligatory one during which one organism, the host, merely provides shelter, support, or transport for the other. Metabolic dependency is not involved. According to this definition, those animals that are commonly referred to as being epizootic or epizoic can be considered as being engaged in phoretic associations with their hosts. Again, in marine biology an example of such a relationship can be cited in the case of fishes of the genus Fierasfer which live within the respiratory tracts of holothurians. Fierasfer is a relatively helpless fish that is readily preyed upon by others. Living in association with the holothurian, which is undisturbed by its presence, Fierasfer is provided with shelter and is transported from place to place. Another example of a phoretic relationship, but one which does not involve transport, is that between the hydroid Clytia balceri and certain intertidal molluscs, such as Donax gouldi and Tivela stultorum in Southern California. The hydroid is attached to the exposed surfaces of the host’s shell and no metabolic dependency occurs. The hydroid presumably does benefit, since it is prevented from being washed away with the tide. Since one of the major criteria employed to distinguish between types of symbioses, specifically to differentiate mutualism and parasitism from commensalism and phoresis, is metabolic dependency, it follows that definite assignments of associations can only be conclusively brought about through physiological and biochemical analyses. Such have been performed on relatively few species although increasingly more information of this nature is being contributed by modern symbiologists. Regrettably, in the case of the symbionts of marine molluscs not much is known other than indirect and inferential evidences. Herein lies a virtually untouched area of research for the imaginative mind. Having given definitions for ytegories of symbioses, it appears appropriate at this point to re-emphasize that overlaps do occur between the types of symbioses described. This is especially true between parasitism and mutualism, which share the feature of the occurrence of metabolic dependency, and between commensalism and phoresis, which do not involve metabolic dependency. The interrelationship between all four categories of symbioses is depicted in Fig. 2. From this diagram, it may be inferred that the greatest amount of overlapping can be expected to occur between commensalism and phoresis at one end, and between parasitism and mutualism at the
8
MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES
other; however, there may also be a slight overlapping between commensalism and parasitism. Cheng (1964b) has discussed the possible origins of symbiotic relationships. It has been concluded that although one type of association may evolve into another, and the occurrence of overlaps suggest this, such need not always be the case. I n certain instances, the types of relationships may also have evolved independently, not involving a transitional stage which could be interpreted as being one of the other established types of symbiosis. NON-OBLICATORY
NON-OBLIOATORY IFACULTATIVE)
IFADULTATWE)
SHARINO OF FOOD
MUTUAL DEPENDENCY
NUMO~IQATORY
ONE-SIDED DEPENDENCY I FACULTATlVE PARASTTISMI
FIQ.2. Diagram illustrating categories of symbioses and overlappings.
Notice that there are greater overlaps between mutualism and parasitism, and between commensalism and phoresis.
11. PREDATION A predatory relationship can be defined as one during which one member, the predator, as a rule, rapidly kills and devours the other, the prey. Furthermore, the two members need not be heterospecific, although they often are.* Another distinction between predator-prey and symbiotic relationships is that, as a rule, a prey reacts towards a predator, commonly attempting to escape from it. Such reactions have been studied in a number of marine invertebrates (Bullock, 1953; Feder, 1963 ; Margolin, 1964a,b ; Gonor, 1965; and others). However, in the case of sedentary prey escape reactions are generally wanting, and hence the use of this criterion in differentiating between symbiotic and predatory relationships is not always effective. The problem is compounded when one considers relationships during which the rapidity of the kill, which is a relative matter, is prolonged. Thus, when relation-
* A predatory relationship involving organisms of the same species is generally recognized as cannibalism.
9
2. DEFINITIONS OF TYPES O P SYMBIOSES
ships between organisms in the marine environment, or in any environment for that matter, are examined, the line of demarcation between parasitism and predation sometimes becomes extremely difficult to recognize. This is especially true if the often used criterion of “ inflicting injury to host ” is employed in defining parasitism, since this would indicate that both predation and parasitism are types of interactions that result in negative effects on the survival of one of the populations. Although this is true with certain parasites, it is by no means the rule as it is with predators. With the acceptance of the definition of parasitism given earlier, the distinction between parasitism and predation becomes more recognizable although the problem is by no means completely resolved. For example, in cases where one member of the association feeds on the tissues of the other and yet does not rapidly destroy the latter, should this be considered as parasitism or predation? It would appear that the solution to this dilemma lies in the qualifying phrase obligatory metabolic dependence ” that is used to define parasitism. If the aggressive member of the association is obligatorily and specifically dependent upon the tissues of the passive member, such a relationship may be categorized as parasitism. However, if the whole or parts of other organisms, within a broad spectrum, may be substituted for the passive member, the association may be considered as a predator-prey relationship. Since this review is only concerned with symbiotic associations, predators of marine molluscs are not considered although a few invertebrates whose role as either parasite or predator remains uncertain are mentioned briefly. (I
DEFINITIONS OF TYPES OF SYMBIOSES I n studying heterospecific associations among organisms, a number of terms have been coined to describe types of relationships. These, however, like so many biological terms, are essentially operational words that are defineable only within broad limits. They are nevertheless useful in that they permit the filing of data into convenient, although in some instances poorly defined and overlapping, compartments. Specifically, the terms symbiosis, parasitism, commensalism, mutualism, inquilinism, phoresis and even predation are often found in the literature pertaining to heterospecific associations. In recent years, various authors (including Lapage, 1958 ; Baer, 1952; Caullery, 1952; Cameron, 1956; Dales, 1957, 1966; Hopkins, 1957b; Yonge, 1957; Dogiel, 1962; Olsen, 1962; Noble and Noble, 1961; Smyth, 1962 ; Sprent, 1963 ; Lincicome, 1963; Cheng, 1964b ; Geiman, 1964; Henry, 1966; Croll, 1966) have presented and discussed definitions for terms that describe heterospecific associations, and, as to be expected, differences, depending upon the immediate interests of the author, exist, sometimes only slightly. I n order that the meanings implied by me in the subsequent pages are clear, those terms that I consider useful are defined below.
I. SYMBIOSIS The term symbiosis, as originally coined by De Bary (1879) to mean no more than " living together ", is being retained in its original sense, although some authors have used symbiosis as a synonym of mutualism. Thus symbiosis is the broad, all-encompassingterm used to describe all types of heterospecific associations, excluding predation, during which there exists physical contact or intimate proximity between the two members. There are no implications of benefit acquirement or giving, nutritional dependency, or infliction or receipt of harm. Thus symbiosis is a broad ecological term under which can be categorized parasitism, commensalism, mutualism and phoresis. AS explained later, I have chosen to consider inquilinism to be no different from commensalism. It is with this or a very'similar definition in mind that Read (1958a) has suggested " a science of symbiosis " and Noble 4
2. DEFINITIONS OF TYPES OF SYMBIOSES
5
and Noble (1961) have expressed the view that because of the modern trends in parasitology, parasitologists might be designated as “ symbiontologists ”. I, however, prefer the term symbiology (Cheng, 196410) over “ symbiontology ”, since the latter implies that the investigator and his discipline are only concerned with one member of the association, the symbiont, and not with the host. As stated earlier, if the study of relationships between heterospecific organisms is to be comprehensive and unique, both the host and the symbiont, plus the nature of the relationship, must be taken into consideration. As stated, several subcategories of symbioses have long been in use in the biological literature. These are redefined below, and are drawn from what are considered to be the most appropriate aspects of previous definitions, although the basic interpretations are those of Smyth (1962).
A. Parasitism Parasitism describes a heterospecific relationship, be it permanent or temporary, during which there exists metabolic dependence of the parasite, the smaller of the two species, on its host. This metabolic dependency may be in the form of nutritional materials, digestive enzymes, developmental stimuli, or control of maturation. With the acceptance of this definition, Smyth (1962) has pointed out that it is now possible “ t o draw up a list of parasitic species which show an increasing degree of metabolic dependence on their hosts ”. Along this hypothetical scale (Fig. l), one can assign free-living organisms to one METABOLICDEPENDENCE Free-living
1
0%
1 Totally parasitic
100%
FIG.1. Diagram showing the relative concept of parasitism based on the degree of metabolic dependence. (After Smyth, 1962.)
terminal and complete dependence, or total parasitism, to the other. It should be pointed out, however, that if the parasite is metabolically dependent on the host even for a single factor, which cannot be obtained from the microenvironment, the relationship becomes an obligatory one if the parasite is to survive and perpetuate its species. Thus “ total dependence ” describes the number of metabolic factors on which the parasite is dependent and not necessarily the extreme at one end of a gradient of relationships.
6
MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES
B. Mutualism Mutualism describes an intimate relationship during which both the mutualist and the host are metabolically dependent on each other. An often cited example of mutualism is that relationship between the cnidarian Chlorohydra viridissima and the green alga Zoochlorella, which lives in the cytoplasm of the nutritive-muscular cells of the cnidarian’s gastrodermis. The alga produces oxygen which Chlorohydra utilizes, and Zoochlorella makes use of the nitrogenous waste products of Chlorohydra for its synthetic processes. Thus there exists interdependency between the mutualist and host. I n addition to this aspect of metabolic dependency, others exist (Muscatine and Lenhoff, 1965a,b ; Muscatine, 1965). What appears to be a concise distinction between parasitism and mutualism has been partially shattered by Smyth’s (1962) viewpoint that mutualism is actually a specialized form of parasitism during which some metabolic by-products of the parasite are of value to the host. Nevertheless, the mutual dependency is a real, recognizable and obligatory one during mutualistic, but not during parasitic, relationships.
C. Commensalism Commensalism describes that type of more or less intimate relationship during which the commensal generally derives physical shelter from the host, is nourished on foods that are associated but not a part of the host, and is not metabolically dependent on the host. Literally, commensalism means “ eating at the same table ”. It is thus a loose type of relationship and is not an obligatory one. I n accepting this definition, there is no longer a need to have a special category of inquilinism as defined by Caullery (1952). One of the best known examples of commensalism is found within the realms of marine biology. This is the association between certain species of hermit crabs and sea anemones. The anemone lives on the shell sheltering the hermit crab, At this location, it benefits directly in that it has access to the food caught and scattered by the crab. I n return, the crab benefits from the presence of the anemone which aids in warding off predators. Yet each animal can live without the other. Not all anemone-hermit crab associations are commensalistic. For example, Faurot (1910) has shown that the relationship between the hermit crab Eupagurus prideauxi and the anemone Adamsia palliata is an obligatory one, since neither of the partners will survive alone. Here the relationship appears to have developed into a mutualistic one.
2. DEFINITIONS O F TYPES O F SYMBIOSES
7
D. Phoresis Phoresis is most akin to commensalism but does not involve “ eating at the same table ”. This type of relationship is again a loose and nonobligatory one during which one organism, the host, merely provides shelter, support, or transport for the other. Metabolic dependency is not involved. According to this definition, those animals that are commonly referred to as being epizootic or epizoic can be considered as being engaged in phoretic associations with their hosts. Again, in marine biology an example of such a relationship can be cited in the case of fishes of the genus Fierasfer which live within the respiratory tracts of holothurians. Fierasfer is a relatively helpless fish that is readily preyed upon by others. Living in association with the holothurian, which is undisturbed by its presence, Fierasfer is provided with shelter and is transported from place to place. Another example of a phoretic relationship, but one which does not involve transport, is that between the hydroid Clytia balceri and certain intertidal molluscs, such as Donax gouldi and Tivela stultorum in Southern California. The hydroid is attached to the exposed surfaces of the host’s shell and no metabolic dependency occurs. The hydroid presumably does benefit, since it is prevented from being washed away with the tide. Since one of the major criteria employed to distinguish between types of symbioses, specifically to differentiate mutualism and parasitism from commensalism and phoresis, is metabolic dependency, it follows that definite assignments of associations can only be conclusively brought about through physiological and biochemical analyses. Such have been performed on relatively few species although increasingly more information of this nature is being contributed by modern symbiologists. Regrettably, in the case of the symbionts of marine molluscs not much is known other than indirect and inferential evidences. Herein lies a virtually untouched area of research for the imaginative mind. Having given definitions for ytegories of symbioses, it appears appropriate at this point to re-emphasize that overlaps do occur between the types of symbioses described. This is especially true between parasitism and mutualism, which share the feature of the occurrence of metabolic dependency, and between commensalism and phoresis, which do not involve metabolic dependency. The interrelationship between all four categories of symbioses is depicted in Fig. 2. From this diagram, it may be inferred that the greatest amount of overlapping can be expected to occur between commensalism and phoresis at one end, and between parasitism and mutualism at the
8
MARINE MOLLUSCS AS HOSTS FOR SYMBIOSES
other; however, there may also be a slight overlapping between commensalism and parasitism. Cheng (1964b) has discussed the possible origins of symbiotic relationships. It has been concluded that although one type of association may evolve into another, and the occurrence of overlaps suggest this, such need not always be the case. I n certain instances, the types of relationships may also have evolved independently, not involving a transitional stage which could be interpreted as being one of the other established types of symbiosis. NON-OBLICATORY
NON-OBLIOATORY IFACULTATIVE)
IFADULTATWE)
SHARINO OF FOOD
MUTUAL DEPENDENCY
NUMO~IQATORY
ONE-SIDED DEPENDENCY I FACULTATlVE PARASTTISMI
FIQ.2. Diagram illustrating categories of symbioses and overlappings.
Notice that there are greater overlaps between mutualism and parasitism, and between commensalism and phoresis.
11. PREDATION A predatory relationship can be defined as one during which one member, the predator, as a rule, rapidly kills and devours the other, the prey. Furthermore, the two members need not be heterospecific, although they often are.* Another distinction between predator-prey and symbiotic relationships is that, as a rule, a prey reacts towards a predator, commonly attempting to escape from it. Such reactions have been studied in a number of marine invertebrates (Bullock, 1953; Feder, 1963 ; Margolin, 1964a,b ; Gonor, 1965; and others). However, in the case of sedentary prey escape reactions are generally wanting, and hence the use of this criterion in differentiating between symbiotic and predatory relationships is not always effective. The problem is compounded when one considers relationships during which the rapidity of the kill, which is a relative matter, is prolonged. Thus, when relation-
* A predatory relationship involving organisms of the same species is generally recognized as cannibalism.
9
2. DEFINITIONS OF TYPES O P SYMBIOSES
ships between organisms in the marine environment, or in any environment for that matter, are examined, the line of demarcation between parasitism and predation sometimes becomes extremely difficult to recognize. This is especially true if the often used criterion of “ inflicting injury to host ” is employed in defining parasitism, since this would indicate that both predation and parasitism are types of interactions that result in negative effects on the survival of one of the populations. Although this is true with certain parasites, it is by no means the rule as it is with predators. With the acceptance of the definition of parasitism given earlier, the distinction between parasitism and predation becomes more recognizable although the problem is by no means completely resolved. For example, in cases where one member of the association feeds on the tissues of the other and yet does not rapidly destroy the latter, should this be considered as parasitism or predation? It would appear that the solution to this dilemma lies in the qualifying phrase obligatory metabolic dependence ” that is used to define parasitism. If the aggressive member of the association is obligatorily and specifically dependent upon the tissues of the passive member, such a relationship may be categorized as parasitism. However, if the whole or parts of other organisms, within a broad spectrum, may be substituted for the passive member, the association may be considered as a predator-prey relationship. Since this review is only concerned with symbiotic associations, predators of marine molluscs are not considered although a few invertebrates whose role as either parasite or predator remains uncertain are mentioned briefly. (I