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Is absence of proof a proof of absence? Comments on commensalism
Palaeogeography, Palaeoclimatology, Palaeoecology 302 (2011) 484–488
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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Is absence of proof a proof of absence? Comments on commensalism Mikołaj K. Zapalski ⁎ University of Warsaw, Faculty of Geology, Żwirki i Wigury 93, 02-089 Warszawa, Poland
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Article history: Received 13 October 2010 Received in revised form 16 January 2011 Accepted 18 January 2011 Available online 25 January 2011 Keywords: Commensalism Parasitism Mutualism Fossil record Null hypothesis in palaeoecology
a b s t r a c t Commensalism in the narrow sense can be understood as an interaction strictly neutral for one organism and positive for the other. Neutral interaction is the absence of interaction and as such it cannot be proven (the proof of absence cannot be made) and consequently it can be regarded as a concept unfit for empirical science. In the broad sense it is often understood as a weak (positive or negative) interaction on one hand and positive on the other. This approach also seems imperfect, as weak interactions should be regarded rather as mutualism or parasitism, respectively. The borders between interactions (commensalism/parasitism and commensalism/mutualism) are difficult to define; hence commensalism should rather be considered as a theoretical interval within the continuum of interactions. Detection of commensalism in recent associations is rather difficult, while in the fossil record it seems impossible. Commensalism as a null hypothesis in paleoecology cannot be retained, as the possibility of making a type II error is very high. The terms “paroecia” and “endoecia” seem to be more useful to use in cases when a particular ecological relationship is difficult to prove. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Commensalism has often been implicitly treated as a null hypothesis in ecology and paleoecology. Biologists can observe living animals with direct live recording of interactions among them; in paleoecology, however, the inconvenient reality is that most of the interactions are lost during taphonomic processes (Tapanila, 2008). The applications of concepts developed by ecology into paleoecology should therefore be taken with care. In the majority of cases interactions between two organisms are not obvious and more developed studies need to be undertaken to recognize them (e. g. Gahn and Baumiller, 2003; Zapalski, 2005). Commensalism has been postulated by numerous authors, and is very often recognized in the fossil record (most recent papers are by de Gibert et al., 2006; Wisshak and Neumann 2006; Ishikawa and Kase, 2007; Zhan and Vinn, 2007; Rodrigues et al., 2008; Martinell and Domènech, 2009; Mõtus and Vinn, 2009; Odin, 2009). Other interactions such as parasitism or mutualism are seldom reported (e. g. Bates and Loydell, 2000; Bassett et al., 2004; Neumann and Wisshak, 2006; Zapalski, 2007; Zapalski and Hubert, 2011; Klug et al., 2011 see also Conway Morris, 1981). Predation, also very commonly recognized interaction in the fossil record (e. g. Ebbestad et al., 2009; Klompmaker et al., 2009; Lindström and Peel, 2010) is not taken into account in this analysis, because it does not involve long coexistence of two organisms; this analysis concerns only symbiotic (sensu lato) relationships.
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It will be shown here that commensalism is nearly impossible to detect in recent associations (due to biological and philosophical premises). Even if it be possible, it has been shown that organisms being temporarily commensal may become parasites or mutualists under the influence of various environmental factors and the character of this relationship can change during the life of individuals. Finally, commensalism has been proposed as a null hypothesis in paleoecology (Tapanila, 2008); it will be shown that this is difficult to follow. 2. Classification of interactions One of several possible classifications of interactions uses the effect of the interaction as a criterion (Lewis, 1985). It can be positive (+), negative (−) or neutral (0) for each organism involved in the relation (Odum and Barrett, 2005; Dobson et al., 2008). The most commonly occurring interactions (such as mutualism or parasitism) require positive or negative effects on each involved organism. Such effects can be of varied intensity — for example a negative effect of the parasite can be expressed as an indistinct illness of the host at one end, and by the host's death at the other. It can be shown on the number line (Fig. 1) that the intensity of a positive interaction can be expressed as (0; ∞), and the range of a negative interaction as (−∞; 0), both excluding zero. The neutral interaction requires a single value, namely 0. A similar presentation was given by Darell and Taylor (1993). In other words, let any two objects be given; interactions between them can be negative, neutral or positive. We have therefore three sets of interactions; positive and negative interactions are continuous
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Fig. 1. Ecological interactions and their effects on involved organisms, expressed on number lines.
and have their magnitude, while neutral interaction has only “0” value. Thus we have positive and negative interactions with broad number of possible values, and neutral interaction with only one possible value.
3. How frequent are interspecific interactions? The probability of finding an element from one of the two large sets is greater than finding the element from a remaining single-value (or single-element) set. Even if all values are not equally probable to occur, we can argue for negative and positive interactions being more common than neutral interaction. Hence, parasitism and mutualism should be recognized much more often than neutral interactions. Having a look at the ISI Web of Knowledge browser it can be found that browsing for “parasit*”, the site returns more than 90 thousand documents; for “mutual*” – more than 40 thousand; finally, for “commensal*” – less than 4 thousand. Most of these papers concern recently living organisms. The latter interaction occurs in this database at an order of magnitude less often than the two former ones. Of course, the database covers various kinds of articles (showing that an organism is not a parasite, for example), but nonetheless gives a general idea as to how often the given interaction is under research – and with some approximation, in consequence – how often it occurs in nature. To support these considerations it can be stated that parasites dominate the ecosystems — some researchers suggest that most of species on Earth are parasites (Windsor, 1998); 75% of links in natural food webs probably involve parasites (Lafferty et al., 2006; Dobson et al., 2008). It can be added that a healthy ecosystem is rich in parasites (Hudson et al., 2006). The fossil record is strongly biased in the terms of biodiversity and anatomy. It can be presumed that ecological relations in the fossil record are biased as well. Surprisingly, out of all symbiotic relationships commensalism is incomparably more often recognized in fossil record than other symbiotic relationships (e. g. Schneider, 2003; Ishikawa and Kase, 2007; Zhan and Vinn, 2007; Tapanila and Ebbestad, 2008; Odin, 2009; Key et al., 2010).
4. Commensalism — biological perspective Papers describing commensalism in modern associations usually argue for it in two ways. The first is simply to assume that if large numbers of symbionts are tolerated by the host, then that means that they are harmless (e. g. Browne and Kingsford, 2005; Dvoretsky and Dvoretsky, 2009). The other way of arguing states that there is very little cost to the host (e. g. Goto et al., 2007; Lee et al., 2009). There are many papers which simply assume commensalism without discussing it (e. g. Steele et al., 1986; Parente and Hendrickx, 2000; Thomas and Klebba, 2007; Kane et al., 2008). Very rare papers state argument for positive effect on one hand and state inability of detecting positive or negative effect on the other — and therefore assuming neutral effect (e. g. Mosher and Watling, 2009). The first argument can be easily rejected by comparison with parasites. Well established parasites are not greatly harmful to the host, the most harmful parasites are usually these having very short common history with their host. Tolerance of parasites is very common in recent host–parasite associations (Miller et al., 2005). Well fit parasites can be tolerated by their hosts even in very large quantities – for example red foxes in Southern Poland are commonly infested by a tapeworm Echinococcus multilocularis – about 86% of the host individuals possess 1–100 parasites, but about 4% have more than 1000 tapeworms (Borecka et al., 2008; see also data on parasite infection in wolves given by Kloch et al., 2005). These tapeworms are undoubtedly tolerated by the host, especially at low infestation rates. And they are undoubtedly parasites (e. g. Gottstein and Hemphill, 2008; Bagrade et al., 2009). Therefore the argument on toleration of high infestation does not support the conclusion on commensalism. Moreover, in the present author's opinion it is methodologically wrong when an interaction is analyzed between the host and endobionts en masse — while the interaction occurs between two individuals, a host and a symbiont. In the quoted example of red foxes (Borecka et al., 2008) it can be imagined that a small number of “commensals” make “very little cost” to the host; at very high infestation rates they “become” parasites, which are really harmful to the host. There is a common argument on
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“commensal” relationships that a “true parasite” must affect either fecundity or body mass/volume of the host (e. g. Nunn and Altizer, 2006; Deter et al., 2007). A single tapeworm will surely not affect the former; and any effect of the latter can be rather undetectable (especially when the parasite is well established and the host organism can be infested by hundreds of parasites). It seems that the concept of commensalism merges gradually into parasitism with the rate of infestation. 5. Commensalism — philosophical perspective There are two possible ways of understanding commensalism, broad and narrow. Broad understanding regards commensalism as an interaction with a positive effect on one, and a weak (either positive or negative) effect on the other. Such an attitude is very subjective and for one researcher “weak” (“very little cost”) can have different meaning than for the other. Where is the point where it is possible to distinguish commensalism from the remaining interactions? The distinction between commensal and parasitic, in many groups of microorganisms in particular, is often far from clear-cut (Miller et al., 2006). It can therefore be seen that even in modern associations “broad” commensalism is very difficult to prove and very difficult to separate from other interactions. Narrow understanding of commensalism considers it as strictly neutral for one of symbionts (Fig. 2). Are there any possibilities to prove a neutral interaction? One of the informal logical fallacies is argumentum ad ignorantiam, where absence of proof is understood as a proof of absence. However, absence of proof as an argument for something cannot be accepted, as one never knows if such an absence is caused by a true absence or only that it is impossible to identify it (proof of absence cannot be made). Commensalism understood in this way can therefore be treated as an empty name (a proper name that does not have a referent). This is probably why neither of the terms “commensalism” nor “amensalism” appear in modern handbooks of ecology (e.g. Case, 2000; Krebs, 2001). Only Odum and Barrett (2005) had shown an example of commensalism, where a small crab inhabits the mantle cave of an oyster. In the same example the authors show that this “commensal” crab can damage its host (Odum and Barrett, 2005, p. 305), therefore the described interaction is not truly neutral. 6. Discussion Commensalism in the “narrow” (i.e., strictly neutral) version cannot be proven due to formal premises. Only “broad” understanding of commensalism could be retained, as faint interactions may be proven and detected. Such understanding of commensalism is useful, but faint interaction is not an absence of interaction; hence – being strict – it is not commensalism, but parasitism or mutualism respectively, depending on the nature of this faint interaction. How can we therefore distinguish commensalism in its “broad” version
from parasitism or mutualism with weak effect? Where should the border between interactions be placed? The gradual change from neutral to positive or negative interaction might be analyzed in terms of multi-valued or fuzzy logic (e.g., Wilkinson, 1963; Wang and Zhou, 2009). It appears, however, that objective methods are difficult to apply to measure gradual change of the value of the interaction. Placement of borders among interactions seems therefore to be elusive; the description becomes not a classification, but a typology. As stated by Miller et al. (2006), species considered commensal may be on the edge of parasitism with some strains causing damage to their hosts. The term “commensalism” is often abused. Organisms classified as commensals are not always really neutral for their host, or their interactions with hosts can fluctuate over time. They can become serious pathogens, as may be in the cases of Fusobacterium varium or Escherichia coli (Ohkusa et al., 2009); similar situations are known also from other “commensal pathogens” (Jouault et al., 2009). Microorganisms potentially neutral for their hosts can quickly become strongly pathogenic (Leavis et al., 2007, see also Drake, 2008); furthermore, human commensals can under certain circumstances become even fatal, and vaccines against these “commensals” are developed (Stephens, 2009). In addition, some microorganisms not harmful for one individual can become pathogenic for the other (Casadevall and Pirofski, 2000; Sachs and Wilcox, 2006). Misuse of the discussed term can lead to confusing statements, as for example “Rhodotorula species are commensal yeasts of variable pathogenicity” (Alliot et al., 2000). Parasitism and mutualism are interactions that may occur at a biochemical level only, and do not need to change the anatomy of the host. They are impossible to detect in the fossil record. Parasitism seems to be a good example of such an interaction. A good illustration of such an interaction is the case of the crab Hemigrapsus crenulatus infested by the acanthocephalan Profilicollis antarcticus. The parasite stimulates production of serotonin, dopamine, and octopamine that affect motor, ventilatory and cardiac activities, behavior and coloration patterns (Haye and Ojeda, 1998, see also Livingstone et al., 1980). Interactions not causing anatomical changes are not taphonomically preservable and may easily be omitted in paleoecological analysis and classified as commensalism (Feldmann et al., 1996). Furthermore, due to the lack of anatomical influence of a symbiont on its host, none of them can be detected in fossil record. Many pathogens evolve in situ from species that are commensals (Ehrlich et al., 2008); according to Leung and Poulin, 2008, intraspecific relations are often unstable and they represent a continuum of interactions. Also Bronstein (1994) observed that the costs and benefits that determine net effects of interactions can vary greatly in both space and time. Lee et al. (2009) described an annelid–crayfish association, in which the interaction may fluctuate between commensalism and mutualism depending on environmental conditions. Such observations may suggest that any unsupported firm statement in paleoecology should be treated with caution, as relationships between individuals
Fig. 2. “Broad” and “narrow” understanding of commensalism. Broad understanding requires faint interaction (positive or negative), but the limits between interactions are blurred, while narrow understanding requires strictly neutral (0) interaction.
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may often be unbalanced and change during their lives (Cheney and Côté, 2005). Commensalism seems to be only a possible point in such a continuum, barely detectable in recent associations. As briefly discussed above, the possibility of detecting commensalism in recent associations is very low, and most of the described “commensal relationships” can be classified within other interactions. How does this observation affect the commensal null hypothesis used in paleoecology (Tapanila, 2008)? Tapanila (2008) proposed several cases where the null hypothesis on commensalism can be rejected; such situations are very rare and in most of situations the null hypothesis would be not rejected. According to Popper's methodology of science (Popper, 1959) the concept of commensalism can therefore be regarded as unverifiable. While testing a hypothesis two types of errors may occur: type I and type II. The type I error occurs when a true null hypothesis is rejected, and a type II error occurs when a false null hypothesis is not rejected. Generally, the smaller the type I error is, the larger the type II error is, and conversely. Commensalism, understood in its narrow definition seems to be exceptional in modern associations. The possibility of making type I error is therefore extremely low (NB. according to Bayes' theorem (Bayes, 1763) the rates of both errors are influenced not only by the accuracy of the test, but also by the frequency of occurrence of the given case in a population), which causes that possibility of making type II error becomes very high and the false null hypothesis is not rejected. The term “commensalism” indicates a relationship that is difficult to prove. There are other, somewhat neglected terms, indicating spatial relationships between organisms, but not denoting ecological interactions between them. The term paroecie (from Greek “living together”) can be used for two organisms occurring in vivo in an association, while endoecie (from Greek “living inside”) for an organism inhabiting cavities of another. These terms are better in cases, where it is impossible to recognize biological relationships between organisms. 7. Conclusions 1. Commensalism in its “narrow” version can be treated as a concept that cannot be proven (empty name), as the absence of proof cannot be regarded as a proof of absence. In consequence it is unfit for experimental science. 2. Its “broad” version is very subjective and its borders with the neighboring kinds of interaction are unclear; moreover, interactions change over time; commensalism should not be treated as a separate interaction, but rather a theoretical interval within the continuum of interactions. 3. Faint interactions can be categorized rather as parasitism or mutualism, depending on case. 4. Detection of commensalism in recent associations seems to be very difficult, while in the fossil record it seems nearly impossible. 5. The null hypothesis on commensalism should not be made due to the very high possibility of making a type II error. 6. Terms “paroecia” and “endoecia” seem to be more useful to use in cases when a particular ecological relationship is difficult to prove. Acknowledgments I am deeply grateful to E. N. K. Clarkson (University of Edinburgh) for comments and linguistical corrections. I would also like to express my gratitude to L. Tapanila (Idaho State University) and U. Radwańska (Warsaw University) for discussions on commensalism and other ecological interactions. A. T. Halamski (Institute of Paleobiology PAS) is thanked for inspiring discussions and critical comments on the manuscript. Michał Kowalewski (Virginia Tech, Blacksburg), a journal referee kindly gave comments that helped to improve this manuscript.
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Palaeogeography, Palaeoclimatology, Palaeoecology j o u r n a l h o m e p a g e : w w w. e l s ev i e r. c o m / l o c a t e / p a l a e o
Is absence of proof a proof of absence? Comments on commensalism Mikołaj K. Zapalski ⁎ University of Warsaw, Faculty of Geology, Żwirki i Wigury 93, 02-089 Warszawa, Poland
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Article history: Received 13 October 2010 Received in revised form 16 January 2011 Accepted 18 January 2011 Available online 25 January 2011 Keywords: Commensalism Parasitism Mutualism Fossil record Null hypothesis in palaeoecology
a b s t r a c t Commensalism in the narrow sense can be understood as an interaction strictly neutral for one organism and positive for the other. Neutral interaction is the absence of interaction and as such it cannot be proven (the proof of absence cannot be made) and consequently it can be regarded as a concept unfit for empirical science. In the broad sense it is often understood as a weak (positive or negative) interaction on one hand and positive on the other. This approach also seems imperfect, as weak interactions should be regarded rather as mutualism or parasitism, respectively. The borders between interactions (commensalism/parasitism and commensalism/mutualism) are difficult to define; hence commensalism should rather be considered as a theoretical interval within the continuum of interactions. Detection of commensalism in recent associations is rather difficult, while in the fossil record it seems impossible. Commensalism as a null hypothesis in paleoecology cannot be retained, as the possibility of making a type II error is very high. The terms “paroecia” and “endoecia” seem to be more useful to use in cases when a particular ecological relationship is difficult to prove. © 2011 Elsevier B.V. All rights reserved.
1. Introduction Commensalism has often been implicitly treated as a null hypothesis in ecology and paleoecology. Biologists can observe living animals with direct live recording of interactions among them; in paleoecology, however, the inconvenient reality is that most of the interactions are lost during taphonomic processes (Tapanila, 2008). The applications of concepts developed by ecology into paleoecology should therefore be taken with care. In the majority of cases interactions between two organisms are not obvious and more developed studies need to be undertaken to recognize them (e. g. Gahn and Baumiller, 2003; Zapalski, 2005). Commensalism has been postulated by numerous authors, and is very often recognized in the fossil record (most recent papers are by de Gibert et al., 2006; Wisshak and Neumann 2006; Ishikawa and Kase, 2007; Zhan and Vinn, 2007; Rodrigues et al., 2008; Martinell and Domènech, 2009; Mõtus and Vinn, 2009; Odin, 2009). Other interactions such as parasitism or mutualism are seldom reported (e. g. Bates and Loydell, 2000; Bassett et al., 2004; Neumann and Wisshak, 2006; Zapalski, 2007; Zapalski and Hubert, 2011; Klug et al., 2011 see also Conway Morris, 1981). Predation, also very commonly recognized interaction in the fossil record (e. g. Ebbestad et al., 2009; Klompmaker et al., 2009; Lindström and Peel, 2010) is not taken into account in this analysis, because it does not involve long coexistence of two organisms; this analysis concerns only symbiotic (sensu lato) relationships.
⁎ Tel.: +48 22 5540473; fax: +48 22 5540001. E-mail address: [email protected]. 0031-0182/$ – see front matter © 2011 Elsevier B.V. All rights reserved. doi:10.1016/j.palaeo.2011.01.013
It will be shown here that commensalism is nearly impossible to detect in recent associations (due to biological and philosophical premises). Even if it be possible, it has been shown that organisms being temporarily commensal may become parasites or mutualists under the influence of various environmental factors and the character of this relationship can change during the life of individuals. Finally, commensalism has been proposed as a null hypothesis in paleoecology (Tapanila, 2008); it will be shown that this is difficult to follow. 2. Classification of interactions One of several possible classifications of interactions uses the effect of the interaction as a criterion (Lewis, 1985). It can be positive (+), negative (−) or neutral (0) for each organism involved in the relation (Odum and Barrett, 2005; Dobson et al., 2008). The most commonly occurring interactions (such as mutualism or parasitism) require positive or negative effects on each involved organism. Such effects can be of varied intensity — for example a negative effect of the parasite can be expressed as an indistinct illness of the host at one end, and by the host's death at the other. It can be shown on the number line (Fig. 1) that the intensity of a positive interaction can be expressed as (0; ∞), and the range of a negative interaction as (−∞; 0), both excluding zero. The neutral interaction requires a single value, namely 0. A similar presentation was given by Darell and Taylor (1993). In other words, let any two objects be given; interactions between them can be negative, neutral or positive. We have therefore three sets of interactions; positive and negative interactions are continuous
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Fig. 1. Ecological interactions and their effects on involved organisms, expressed on number lines.
and have their magnitude, while neutral interaction has only “0” value. Thus we have positive and negative interactions with broad number of possible values, and neutral interaction with only one possible value.
3. How frequent are interspecific interactions? The probability of finding an element from one of the two large sets is greater than finding the element from a remaining single-value (or single-element) set. Even if all values are not equally probable to occur, we can argue for negative and positive interactions being more common than neutral interaction. Hence, parasitism and mutualism should be recognized much more often than neutral interactions. Having a look at the ISI Web of Knowledge browser it can be found that browsing for “parasit*”, the site returns more than 90 thousand documents; for “mutual*” – more than 40 thousand; finally, for “commensal*” – less than 4 thousand. Most of these papers concern recently living organisms. The latter interaction occurs in this database at an order of magnitude less often than the two former ones. Of course, the database covers various kinds of articles (showing that an organism is not a parasite, for example), but nonetheless gives a general idea as to how often the given interaction is under research – and with some approximation, in consequence – how often it occurs in nature. To support these considerations it can be stated that parasites dominate the ecosystems — some researchers suggest that most of species on Earth are parasites (Windsor, 1998); 75% of links in natural food webs probably involve parasites (Lafferty et al., 2006; Dobson et al., 2008). It can be added that a healthy ecosystem is rich in parasites (Hudson et al., 2006). The fossil record is strongly biased in the terms of biodiversity and anatomy. It can be presumed that ecological relations in the fossil record are biased as well. Surprisingly, out of all symbiotic relationships commensalism is incomparably more often recognized in fossil record than other symbiotic relationships (e. g. Schneider, 2003; Ishikawa and Kase, 2007; Zhan and Vinn, 2007; Tapanila and Ebbestad, 2008; Odin, 2009; Key et al., 2010).
4. Commensalism — biological perspective Papers describing commensalism in modern associations usually argue for it in two ways. The first is simply to assume that if large numbers of symbionts are tolerated by the host, then that means that they are harmless (e. g. Browne and Kingsford, 2005; Dvoretsky and Dvoretsky, 2009). The other way of arguing states that there is very little cost to the host (e. g. Goto et al., 2007; Lee et al., 2009). There are many papers which simply assume commensalism without discussing it (e. g. Steele et al., 1986; Parente and Hendrickx, 2000; Thomas and Klebba, 2007; Kane et al., 2008). Very rare papers state argument for positive effect on one hand and state inability of detecting positive or negative effect on the other — and therefore assuming neutral effect (e. g. Mosher and Watling, 2009). The first argument can be easily rejected by comparison with parasites. Well established parasites are not greatly harmful to the host, the most harmful parasites are usually these having very short common history with their host. Tolerance of parasites is very common in recent host–parasite associations (Miller et al., 2005). Well fit parasites can be tolerated by their hosts even in very large quantities – for example red foxes in Southern Poland are commonly infested by a tapeworm Echinococcus multilocularis – about 86% of the host individuals possess 1–100 parasites, but about 4% have more than 1000 tapeworms (Borecka et al., 2008; see also data on parasite infection in wolves given by Kloch et al., 2005). These tapeworms are undoubtedly tolerated by the host, especially at low infestation rates. And they are undoubtedly parasites (e. g. Gottstein and Hemphill, 2008; Bagrade et al., 2009). Therefore the argument on toleration of high infestation does not support the conclusion on commensalism. Moreover, in the present author's opinion it is methodologically wrong when an interaction is analyzed between the host and endobionts en masse — while the interaction occurs between two individuals, a host and a symbiont. In the quoted example of red foxes (Borecka et al., 2008) it can be imagined that a small number of “commensals” make “very little cost” to the host; at very high infestation rates they “become” parasites, which are really harmful to the host. There is a common argument on
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“commensal” relationships that a “true parasite” must affect either fecundity or body mass/volume of the host (e. g. Nunn and Altizer, 2006; Deter et al., 2007). A single tapeworm will surely not affect the former; and any effect of the latter can be rather undetectable (especially when the parasite is well established and the host organism can be infested by hundreds of parasites). It seems that the concept of commensalism merges gradually into parasitism with the rate of infestation. 5. Commensalism — philosophical perspective There are two possible ways of understanding commensalism, broad and narrow. Broad understanding regards commensalism as an interaction with a positive effect on one, and a weak (either positive or negative) effect on the other. Such an attitude is very subjective and for one researcher “weak” (“very little cost”) can have different meaning than for the other. Where is the point where it is possible to distinguish commensalism from the remaining interactions? The distinction between commensal and parasitic, in many groups of microorganisms in particular, is often far from clear-cut (Miller et al., 2006). It can therefore be seen that even in modern associations “broad” commensalism is very difficult to prove and very difficult to separate from other interactions. Narrow understanding of commensalism considers it as strictly neutral for one of symbionts (Fig. 2). Are there any possibilities to prove a neutral interaction? One of the informal logical fallacies is argumentum ad ignorantiam, where absence of proof is understood as a proof of absence. However, absence of proof as an argument for something cannot be accepted, as one never knows if such an absence is caused by a true absence or only that it is impossible to identify it (proof of absence cannot be made). Commensalism understood in this way can therefore be treated as an empty name (a proper name that does not have a referent). This is probably why neither of the terms “commensalism” nor “amensalism” appear in modern handbooks of ecology (e.g. Case, 2000; Krebs, 2001). Only Odum and Barrett (2005) had shown an example of commensalism, where a small crab inhabits the mantle cave of an oyster. In the same example the authors show that this “commensal” crab can damage its host (Odum and Barrett, 2005, p. 305), therefore the described interaction is not truly neutral. 6. Discussion Commensalism in the “narrow” (i.e., strictly neutral) version cannot be proven due to formal premises. Only “broad” understanding of commensalism could be retained, as faint interactions may be proven and detected. Such understanding of commensalism is useful, but faint interaction is not an absence of interaction; hence – being strict – it is not commensalism, but parasitism or mutualism respectively, depending on the nature of this faint interaction. How can we therefore distinguish commensalism in its “broad” version
from parasitism or mutualism with weak effect? Where should the border between interactions be placed? The gradual change from neutral to positive or negative interaction might be analyzed in terms of multi-valued or fuzzy logic (e.g., Wilkinson, 1963; Wang and Zhou, 2009). It appears, however, that objective methods are difficult to apply to measure gradual change of the value of the interaction. Placement of borders among interactions seems therefore to be elusive; the description becomes not a classification, but a typology. As stated by Miller et al. (2006), species considered commensal may be on the edge of parasitism with some strains causing damage to their hosts. The term “commensalism” is often abused. Organisms classified as commensals are not always really neutral for their host, or their interactions with hosts can fluctuate over time. They can become serious pathogens, as may be in the cases of Fusobacterium varium or Escherichia coli (Ohkusa et al., 2009); similar situations are known also from other “commensal pathogens” (Jouault et al., 2009). Microorganisms potentially neutral for their hosts can quickly become strongly pathogenic (Leavis et al., 2007, see also Drake, 2008); furthermore, human commensals can under certain circumstances become even fatal, and vaccines against these “commensals” are developed (Stephens, 2009). In addition, some microorganisms not harmful for one individual can become pathogenic for the other (Casadevall and Pirofski, 2000; Sachs and Wilcox, 2006). Misuse of the discussed term can lead to confusing statements, as for example “Rhodotorula species are commensal yeasts of variable pathogenicity” (Alliot et al., 2000). Parasitism and mutualism are interactions that may occur at a biochemical level only, and do not need to change the anatomy of the host. They are impossible to detect in the fossil record. Parasitism seems to be a good example of such an interaction. A good illustration of such an interaction is the case of the crab Hemigrapsus crenulatus infested by the acanthocephalan Profilicollis antarcticus. The parasite stimulates production of serotonin, dopamine, and octopamine that affect motor, ventilatory and cardiac activities, behavior and coloration patterns (Haye and Ojeda, 1998, see also Livingstone et al., 1980). Interactions not causing anatomical changes are not taphonomically preservable and may easily be omitted in paleoecological analysis and classified as commensalism (Feldmann et al., 1996). Furthermore, due to the lack of anatomical influence of a symbiont on its host, none of them can be detected in fossil record. Many pathogens evolve in situ from species that are commensals (Ehrlich et al., 2008); according to Leung and Poulin, 2008, intraspecific relations are often unstable and they represent a continuum of interactions. Also Bronstein (1994) observed that the costs and benefits that determine net effects of interactions can vary greatly in both space and time. Lee et al. (2009) described an annelid–crayfish association, in which the interaction may fluctuate between commensalism and mutualism depending on environmental conditions. Such observations may suggest that any unsupported firm statement in paleoecology should be treated with caution, as relationships between individuals
Fig. 2. “Broad” and “narrow” understanding of commensalism. Broad understanding requires faint interaction (positive or negative), but the limits between interactions are blurred, while narrow understanding requires strictly neutral (0) interaction.
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may often be unbalanced and change during their lives (Cheney and Côté, 2005). Commensalism seems to be only a possible point in such a continuum, barely detectable in recent associations. As briefly discussed above, the possibility of detecting commensalism in recent associations is very low, and most of the described “commensal relationships” can be classified within other interactions. How does this observation affect the commensal null hypothesis used in paleoecology (Tapanila, 2008)? Tapanila (2008) proposed several cases where the null hypothesis on commensalism can be rejected; such situations are very rare and in most of situations the null hypothesis would be not rejected. According to Popper's methodology of science (Popper, 1959) the concept of commensalism can therefore be regarded as unverifiable. While testing a hypothesis two types of errors may occur: type I and type II. The type I error occurs when a true null hypothesis is rejected, and a type II error occurs when a false null hypothesis is not rejected. Generally, the smaller the type I error is, the larger the type II error is, and conversely. Commensalism, understood in its narrow definition seems to be exceptional in modern associations. The possibility of making type I error is therefore extremely low (NB. according to Bayes' theorem (Bayes, 1763) the rates of both errors are influenced not only by the accuracy of the test, but also by the frequency of occurrence of the given case in a population), which causes that possibility of making type II error becomes very high and the false null hypothesis is not rejected. The term “commensalism” indicates a relationship that is difficult to prove. There are other, somewhat neglected terms, indicating spatial relationships between organisms, but not denoting ecological interactions between them. The term paroecie (from Greek “living together”) can be used for two organisms occurring in vivo in an association, while endoecie (from Greek “living inside”) for an organism inhabiting cavities of another. These terms are better in cases, where it is impossible to recognize biological relationships between organisms. 7. Conclusions 1. Commensalism in its “narrow” version can be treated as a concept that cannot be proven (empty name), as the absence of proof cannot be regarded as a proof of absence. In consequence it is unfit for experimental science. 2. Its “broad” version is very subjective and its borders with the neighboring kinds of interaction are unclear; moreover, interactions change over time; commensalism should not be treated as a separate interaction, but rather a theoretical interval within the continuum of interactions. 3. Faint interactions can be categorized rather as parasitism or mutualism, depending on case. 4. Detection of commensalism in recent associations seems to be very difficult, while in the fossil record it seems nearly impossible. 5. The null hypothesis on commensalism should not be made due to the very high possibility of making a type II error. 6. Terms “paroecia” and “endoecia” seem to be more useful to use in cases when a particular ecological relationship is difficult to prove. Acknowledgments I am deeply grateful to E. N. K. Clarkson (University of Edinburgh) for comments and linguistical corrections. I would also like to express my gratitude to L. Tapanila (Idaho State University) and U. Radwańska (Warsaw University) for discussions on commensalism and other ecological interactions. A. T. Halamski (Institute of Paleobiology PAS) is thanked for inspiring discussions and critical comments on the manuscript. Michał Kowalewski (Virginia Tech, Blacksburg), a journal referee kindly gave comments that helped to improve this manuscript.
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