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Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts
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Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts
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Karla Magalhães Campião a,⇑, Augusto Cesar de Aquino Ribas b, Stephen J. Cornell b, Michael Begon c, Luiz Eduardo Roland Tavares d a
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal do Paraná, Brazil Faculdade de Computação, Universidade Federal de Mato Grosso do Sul, Brazil Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK d Centro de Ciências Biológicas e da Saúde, Universidade Federal de Mato Grosso do Sul, Brazil b c
a r t i c l e
i n f o
Article history: Received 27 May 2015 Received in revised form 20 August 2015 Accepted 24 August 2015 Available online xxxx Keywords: Coextinction Specialist Host Anura Parasite Species loss Biodiversity
a b s t r a c t Amphibians are known as the most threatened vertebrate group. One of the outcomes of a species’ extinction is the coextinction of its dependents. Here, we estimate the extinction risk of helminth parasites of South America anurans. Parasite coextinction probabilities were modeled, assuming parasite specificity and host vulnerability to extinction as determinants. Parasite species associated with few hosts were the most prone to extinction, and extinction risk varied amongst helminth species of different taxonomic groups and life cycle complexity. Considering host vulnerability in the model decreased the extinction probability of most parasites species. However, parasite specificity and host vulnerability combined to increase the extinction probabilities of 44% of the helminth species reported in a single anuran species. Ó 2015 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc.
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Biodiversity is declining at alarming rates, similar to those of historical mass extinctions (Stork, 2010). Rapid changes in atmospheric conditions, habitat fragmentation, pollution, invasive species and pathogens, individually and collectively, represent a greater threat to existence than most living species have previously experienced (Barnosky et al., 2011). Amphibians are much affected by the current biodiversity crisis, with well-documented recent extinctions in response to such stressors (Pounds et al., 2006). At least 32% of existing amphibians are at threat from extinction (Stuart et al., 2004) and numerous populations are facing major population declines, morphological deformities and severe pathogen infections (Daszak et al., 2003). One of the outcomes of a species’ extinction is the coextinction of its dependants, which is one of the most common, but least understood, routes to biodiversity loss (Brook et al., 2008; Dunn et al., 2009). When one thinks about extinction, parasite species are generally seen as one of the threats that free-living organisms have to face in a changing world. However, parasite species may be ⇑ Corresponding author at: Programa de Pós Graduação em Ecologia e Conservação, Departamento de Zoologia, Universidade Federal do Paraná, 81531-980 Curitiba, PR, Brazil. Tel.: +55 41 3361 1595. E-mail address: [email protected] (K.M. Campião).
more prone to, and affected by, extinction than free-living organisms (Moir et al., 2011). Parasite extinction may first seem beneficial to hosts, especially those endangered, but some long-term consequences might be severely disadvantageous, such as a loss of genetic diversity of their hosts or increased abundance of other pathogenic parasites (Altizer et al., 2003; Dobson et al., 2008). For instance, Altizer et al. (2003) showed that exposure to parasites maintains host allelic diversity and sexual recombination, which is related to resistance and immune defence against pathogens in a wide range of host species. Parasite diversity is also linked to ecosystem health, as parasite species richness affects the robustness, stability and persistence of food webs (Dunne et al., 2013; McQuaid and Britton, 2014). Coextinctions are often difficult to document and models estimating coextinction rates may therefore be useful in predicting and preventing future biodiversity loss (Colwell et al., 2012). These estimates are influenced by host and parasite traits and by the interactions between them. The degree of host specificity is a key factor in determining coextinction risk, since parasites with restricted host relationships are more likely to become extinct with their hosts (Dobson et al., 2008; Lafferty, 2012). Parasite extinction likelihood may also vary with their host’s vulnerability to extinction (Lafferty, 2012). Hence, assuming that extinctions are not
http://dx.doi.org/10.1016/j.ijpara.2015.08.010 0020-7519/Ó 2015 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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random in nature, and that hosts vary in their likelihood of becoming extinct, provides a more realistic scenario of how parasite biodiversity will respond to host extinctions (Moir et al., 2010). Here, we use data on the helminth parasites of South American anurans to explore the relationships between parasite specificity and host vulnerability in determining parasite coextinction rates. We compiled reports of helminth parasites of amphibians from South America from a recently published list (Campião et al., 2014). This list reports 298 helminth taxa in 186 amphibian species. We conducted the analysis with amphibians of the order Anura only, and excluded all reports in which the host or parasite were not identified to species. It was assumed that a parasite species would persist if at least one of its host species persists. Assuming that host extinction events are statistically independent (Sodhi et al., 2008), this means that the probability Qi that parasite species i persists can be expressed as
Qi ¼ 1 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139
140
ð1 qj Þ;
j2Hi
where qj is the probability that host species j is extant and the product runs over the set Hi of all hosts of parasite species i. We modeled host extinction as a Markov process with rate rj , i.e. we assumed that the probability that the species becomes extinct in the time interval (t, t + dt), provided it is extant at time t, is r j dt. This means that the probability that host species j is extant after time t dqj dt
satisfies ¼ rj qj ; and by solving this we find that that the probability qj ðtÞ is given by erj t . By assuming particular relationships between the host extinction rate rj and host traits, we were able to study how parasite extinction probabilities varied under different scenarios for host extinction. The anuran geographic range was adopted as a measure of host vulnerability and this was modeled as rj ¼ c=logðAj Þ, where Aj is the geographic range of species j and c is a constant. This means that the chance of that species becoming extinct increases as geo
ct
graphic range declines and qj ðtÞ is now given by e logðAj Þ . Several other factors might be important in determining amphibians’ vulnerability to extinction. Here, we focused on geographic range because it is positively correlated to species’ niche breadth and abundance (Slatyer et al., 2013), being the most important driver of amphibian extinction risk (Sodhi et al., 2008; Cooper et al., 2011; Whitton et al., 2012; Ficetola et al., 2015), and is known for all host species in the dataset. Geographic range data were compiled from International Union for Conservation of Nature (IUCN, http://www.iucnredlist.org/technical-documents/spatialdata) records. We do not have any specific information on the time scale for host extinction, so we are unable to estimate the constant c that determines the extinction rates. Rather than choosing explicit but arbitrary values for c and t, and determining the probability of parasites becoming extinct after this time, we instead assumed that a particular fraction of the hosts had become extinct. As described above, the probability that host j is extant at time t is qj ðtÞ, so the mean number of extant host species after time t is
SðtÞ ¼ 142
Y
X X ct qj ðtÞ ¼ e logðAj Þ ; j
particularly high or low extinction probabilities, given its number of hosts. To do this, bootstrap distributions of the extinction probabilities were generated by randomly resampling, with replacement, the geographic ranges Aj (and, hence, extinction rates r j ) of the host species. This allows testing of the null hypothesis that there is no association between host vulnerability and particular parasite species or groups. To assess the effect of host vulnerability on the extinction probabilities of the parasite species, the observed estimates were tested to confirm whether those had a significant tendency to be greater or smaller than the medians of the bootstrap confidence intervals (CIs), using a chi-square test. Differences amongst parasite taxonomic groups (Acanthocephala, Cestoda, Monogenea, Nematoda, Trematoda) were tested with a Fisher’s exact test. A re-sampling (permutation) process was used to compare the extinction probabilities amongst helminth taxonomic groups, and between species with direct and indirect life cycles. This was tested with a re-sampling ANOVA, where we considered different percentages of host species becoming extinct, and a nested relationship between helminth life cycle and taxonomic group. We did 1000 re-samplings, with replacement. Since information on the life cycle of anuran parasites is scarce, the literature was searched for each family and it was assumed that all helminths of a given family would have the same type of life cycle, i.e. direct or indirect. This analysis was conducted with 181 helminth species, because some species in the dataset are inquenda or insertae sedis and were removed. The data set comprised 157 anurans and 194 helminth species. The number of hosts to which a parasite is associated (parasite specificity from here on) was on average 3.7 (SD = 6.68); 52% of the helminth species were associated with a single host species. Monogenea were the most specialised parasites, while Nematoda were the most generalist (Table 1). Parasite species associated with few hosts had higher extinction probabilities (Fig. 1). The vulnerability of hosts associated with specialist (one host) parasites did not differ from other hosts (U = 2670, P = 0.5638). Notwithstanding, 75% of the extinction probabilities generated by the null model were higher than expected if the actual geographic range of each host species was considered (v2 = 45.55, degrees of freedom (df) = 1, P < 0.001). This indicates that most helminths depend on hosts with a higher than average vulnerability to extinction. However, 44% of the specialist parasites had significantly greater extinction probabilities (v2 = 6.01, df = 2, P = 0.049), with Monogenea being the parasite group most negatively affected by their hosts’ vulnerability (i.e. extinction probability was increased; Fisher’s Exact Test for Count Data P = 0.02). Forty-six percent of the helminth species reported have a direct life cycle. Hence, extinction probabilities varied amongst helminth species of different taxonomic groups and life cycle complexity (Fig. 2) with a significant interaction between these factors (Table 2). Therefore, the extinction probabilities tended to be
Table 1 Number of hosts reported in helminth species of different taxonomic groups of parasites from South American anurans.
j
Reported hosts 143 144 145 146 147 148 149 150 151
where the sum runs over all host species. Both qj ðtÞ and SðtÞ depend only on the product ct, so a non-linear equation solver can be used to numerically find the value of ct corresponding to a particular value of SðtÞ, and hence determine the parasite’s extinction probabilities at the point when a particular number of host extinctions have taken place. We used Mann–Whitney U tests to compare extinction rates between different parasite specificity groups (generalists and specialists). We also tested whether a parasites species had
Number of helminth species in each taxonomic group A
C
M
N
T
1 2 >2
2 0 3
6 1 1
10 1 0
58 14 33
35 12 18
Total
5
8
11
105
65
Mean of reported hosts (±S.D.)
3.4 ± 2.6
2.1 ± 2.61
1.1 ± 0.28
3.9 ± 7.53
2.2 ± 2.1
A, Acanthocephala; C, Cestoda; M, Monogenea; N, Nematoda; T, Trematoda.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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Fig. 1. Relation of parasite specificity (number of hosts) and extinction probability of helminth parasites of South American anurans. Lines represent different extinction scenarios that vary with the number of extant anuran species.
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higher in parasites with a direct life cycle, but this is probably because the most specialised parasites, i.e. the monogeneans, have a direct life cycle.
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Our estimates confirmed specialist parasites as the most vulnerable to coextinction. Because parasites ultimately need their hosts for persistence, the number of host species a parasite is associated with is the most crucial parasite trait determining its risk of extinction (Moir et al., 2010). Hence, parasites that exploit different host species have the advantage of being less threatened by extinction, but this comes with the cost of overcoming the physiological and behavioural resistance of different hosts. Although this trade-off seems clear, the course to identify the extent of parasite specificity remains challenging. Many parasite species considered restricted to a narrow set of hosts might occur in other unsampled hosts, which leads to the overestimation of their extinction probabilities (see Brooks et al., 2006 for broader perspective on parasite specificity). On the other hand, extinction probability of generalist parasites may be underestimated by at least two means. First, our model assumes parasites exploited all host species equally, which is a simplification of what actually occurs. Generalist parasites may have a preferred host, whose extinction could affect parasite fitness in a way that would subsequently lead to its extinction (Streicker et al., 2013). Secondly, recent evidence has revealed that generalist parasite species may actually be subsets of cryptic specialists (Keeney et al., 2014; Selbach et al., 2015). Cryptic species are morphologically similar and can only be distinguished by molecular data (Bray and Cribb, 2015). These have been commonly found amongst parasites, because they often have large populations and undergo rapid evolution, which may favour cryptic speciation (Xavier et al., 2015). Thus, the fraction of generalist parasites in our data may comprise a subset of cryptic helminth diversity, since most reports did not include molecular investigations. This would imply
Fig. 2. Estimates of coextinction probabilities of helminth parasites of South American anurans. Letters represent helminth groups: A, Acanthocephala; C, Cestoda; M, Monogenea; N, Nematoda and T, Trematoda. Box plots indicate median lines, 25th and 75th percentiles, with whiskers denoting the 1.5 interquartile ranges and points indicating outliers.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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Table 2 Nested ANOVA comparing the effect of host species extinction amongst helminth species with direct and indirect life cycles, and the major taxonomic groups (Acanthocephala, Monogenea, Cestoda, Nematoda, Trematoda). Variables Extinct host species (%) Life cycle type (direct/indirect) Life cycle/helminth taxonomic group Residuals
Sum of squares
Mean squares
F value
Pa
1 1 3
63.86 0.18 1.17
63.86 0.18 0.39
1954.14 5.68 11.96
0.00 0.02 0.00
899
29.38
0.03
df
df, degrees of freedom. a P value was determined based on 1000 re-samplings.
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that with the higher coextinction probabilities for the species analysed here, and as mentioned by Dobson et al. (2008), a considerable fraction of helminth diversity may become extinct before being identified and classified. For most parasites, the chance of coextinction was decreased by additionally taking their host’s vulnerability to extinction into consideration (i.e. their geographic range). However, the effect was least marked amongst specialist parasites. Since host vulnerability in our null model is assigned at random from the empirical set of vulnerabilities, this suggests that generalist parasites depend on hosts that are more vulnerable than average, whereas specialist parasites do not. Indeed, we found that the vulnerabilities of hosts of specialist parasites were not significantly different from those of other hosts. A recent study on a global fish–parasite interaction network found that the most specialised species tended to occur in nonthreatened hosts, minimising their extinction risks (Strona et al., 2013). We found different results for anurans. Specialised parasites are as likely to occur in vulnerable hosts as are the generalists, being therefore the most prone to extinction. Powell (2011) found similar results in an insect–plant mutualist system, which did not support reduced specialisation of dependent species on the threatened hosts. Additionally, Powell (2011) observed that the densities of dependants in the threatened hosts were lower, suggesting they might become extinct earlier, as a response to lower abundance of a particular a host. Therefore, the extinction rates of parasite species could exceed the number of extinctions of free-living organisms, and parasites may become extinct more rapidly than their hosts (Koh et al., 2004; Dunn et al., 2009; Lafferty, 2012). This is of particular concern for amphibians, a vertebrate group with a high number of threatened species (threat stats available at http://www.iucnredlist.org/), implying that a considerable number of parasites might become extinct even before being discovered. Moreover, considering that helminth parasite diversity can contribute to a decrease in the disease risk in anurans (Johnson et al., 2013), the loss of parasite species could have unpredictable consequences in amphibian conservation and ecosystem health. The extinction probabilities in this analysis tended to be higher for parasites with direct life cycles, but this might not hold if their intermediate hosts were taken into account. Complex life-cycle parasites depend, additionally, on the persistence of their intermediate hosts, and could become extinct due to the lack of such hosts even if their definitive anuran host is not endangered (Lafferty, 2012). Nonetheless, it has been suggested that parasites are able to include, change, or even reduce the number of hosts required to complete their life cycle (Poulin and Cribb, 2002; Parker et al., 2003), which could potentially increase their chances of survival in a host extinction scenario. The variation in extinction probabilities between direct and indirect life cycles may be explained by the most specialised parasites having direct life cycles, eg the monogeneans. Thus, coextinction probabilities vary according to life cycle complexity and
are strongly influenced by parasite specificity, which in turn varies amongst taxonomic groups. This suggests that the coextinction probabilities for helminth parasites are phylogenetically constrained. In contrast, the hosts’ extinction probabilities might not be phylogenetically constrained. A study of the correlates of amphibian extinction risk revealed that the effect of phylogeny is weak, and geographic range is the best predictor (Sodhi et al., 2008). This suggests that in an anuran-helminth system, host vulnerability is mostly affected by extrinsic factors (i.e. habitat degradation), while the main driver of parasite risk is intrinsic (specificity). Overall, we found that the host specificity of parasites and the vulnerability of their hosts combine to determine the coextinction risks of anuran helminth parasites. They interact differently in different parasite taxonomic groups, and the most specialised groups are the most endangered.
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We are grateful to Raul Costa Pereira for his help with data acquisition. K.M.C. and L.E.R.T. received fellowship grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, Brazil), respectively.
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Succinctus
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Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts
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Karla Magalhães Campião a,⇑, Augusto Cesar de Aquino Ribas b, Stephen J. Cornell b, Michael Begon c, Luiz Eduardo Roland Tavares d a
Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal do Paraná, Brazil Faculdade de Computação, Universidade Federal de Mato Grosso do Sul, Brazil Institute of Integrative Biology, University of Liverpool, Liverpool L69 7ZB, UK d Centro de Ciências Biológicas e da Saúde, Universidade Federal de Mato Grosso do Sul, Brazil b c
a r t i c l e
i n f o
Article history: Received 27 May 2015 Received in revised form 20 August 2015 Accepted 24 August 2015 Available online xxxx Keywords: Coextinction Specialist Host Anura Parasite Species loss Biodiversity
a b s t r a c t Amphibians are known as the most threatened vertebrate group. One of the outcomes of a species’ extinction is the coextinction of its dependents. Here, we estimate the extinction risk of helminth parasites of South America anurans. Parasite coextinction probabilities were modeled, assuming parasite specificity and host vulnerability to extinction as determinants. Parasite species associated with few hosts were the most prone to extinction, and extinction risk varied amongst helminth species of different taxonomic groups and life cycle complexity. Considering host vulnerability in the model decreased the extinction probability of most parasites species. However, parasite specificity and host vulnerability combined to increase the extinction probabilities of 44% of the helminth species reported in a single anuran species. Ó 2015 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc.
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Biodiversity is declining at alarming rates, similar to those of historical mass extinctions (Stork, 2010). Rapid changes in atmospheric conditions, habitat fragmentation, pollution, invasive species and pathogens, individually and collectively, represent a greater threat to existence than most living species have previously experienced (Barnosky et al., 2011). Amphibians are much affected by the current biodiversity crisis, with well-documented recent extinctions in response to such stressors (Pounds et al., 2006). At least 32% of existing amphibians are at threat from extinction (Stuart et al., 2004) and numerous populations are facing major population declines, morphological deformities and severe pathogen infections (Daszak et al., 2003). One of the outcomes of a species’ extinction is the coextinction of its dependants, which is one of the most common, but least understood, routes to biodiversity loss (Brook et al., 2008; Dunn et al., 2009). When one thinks about extinction, parasite species are generally seen as one of the threats that free-living organisms have to face in a changing world. However, parasite species may be ⇑ Corresponding author at: Programa de Pós Graduação em Ecologia e Conservação, Departamento de Zoologia, Universidade Federal do Paraná, 81531-980 Curitiba, PR, Brazil. Tel.: +55 41 3361 1595. E-mail address: [email protected] (K.M. Campião).
more prone to, and affected by, extinction than free-living organisms (Moir et al., 2011). Parasite extinction may first seem beneficial to hosts, especially those endangered, but some long-term consequences might be severely disadvantageous, such as a loss of genetic diversity of their hosts or increased abundance of other pathogenic parasites (Altizer et al., 2003; Dobson et al., 2008). For instance, Altizer et al. (2003) showed that exposure to parasites maintains host allelic diversity and sexual recombination, which is related to resistance and immune defence against pathogens in a wide range of host species. Parasite diversity is also linked to ecosystem health, as parasite species richness affects the robustness, stability and persistence of food webs (Dunne et al., 2013; McQuaid and Britton, 2014). Coextinctions are often difficult to document and models estimating coextinction rates may therefore be useful in predicting and preventing future biodiversity loss (Colwell et al., 2012). These estimates are influenced by host and parasite traits and by the interactions between them. The degree of host specificity is a key factor in determining coextinction risk, since parasites with restricted host relationships are more likely to become extinct with their hosts (Dobson et al., 2008; Lafferty, 2012). Parasite extinction likelihood may also vary with their host’s vulnerability to extinction (Lafferty, 2012). Hence, assuming that extinctions are not
http://dx.doi.org/10.1016/j.ijpara.2015.08.010 0020-7519/Ó 2015 Published by Elsevier Ltd. on behalf of Australian Society for Parasitology Inc.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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random in nature, and that hosts vary in their likelihood of becoming extinct, provides a more realistic scenario of how parasite biodiversity will respond to host extinctions (Moir et al., 2010). Here, we use data on the helminth parasites of South American anurans to explore the relationships between parasite specificity and host vulnerability in determining parasite coextinction rates. We compiled reports of helminth parasites of amphibians from South America from a recently published list (Campião et al., 2014). This list reports 298 helminth taxa in 186 amphibian species. We conducted the analysis with amphibians of the order Anura only, and excluded all reports in which the host or parasite were not identified to species. It was assumed that a parasite species would persist if at least one of its host species persists. Assuming that host extinction events are statistically independent (Sodhi et al., 2008), this means that the probability Qi that parasite species i persists can be expressed as
Qi ¼ 1 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124 125 126 127 128 129 130 131 132 133 134 135 136 137 138 139
140
ð1 qj Þ;
j2Hi
where qj is the probability that host species j is extant and the product runs over the set Hi of all hosts of parasite species i. We modeled host extinction as a Markov process with rate rj , i.e. we assumed that the probability that the species becomes extinct in the time interval (t, t + dt), provided it is extant at time t, is r j dt. This means that the probability that host species j is extant after time t dqj dt
satisfies ¼ rj qj ; and by solving this we find that that the probability qj ðtÞ is given by erj t . By assuming particular relationships between the host extinction rate rj and host traits, we were able to study how parasite extinction probabilities varied under different scenarios for host extinction. The anuran geographic range was adopted as a measure of host vulnerability and this was modeled as rj ¼ c=logðAj Þ, where Aj is the geographic range of species j and c is a constant. This means that the chance of that species becoming extinct increases as geo
ct
graphic range declines and qj ðtÞ is now given by e logðAj Þ . Several other factors might be important in determining amphibians’ vulnerability to extinction. Here, we focused on geographic range because it is positively correlated to species’ niche breadth and abundance (Slatyer et al., 2013), being the most important driver of amphibian extinction risk (Sodhi et al., 2008; Cooper et al., 2011; Whitton et al., 2012; Ficetola et al., 2015), and is known for all host species in the dataset. Geographic range data were compiled from International Union for Conservation of Nature (IUCN, http://www.iucnredlist.org/technical-documents/spatialdata) records. We do not have any specific information on the time scale for host extinction, so we are unable to estimate the constant c that determines the extinction rates. Rather than choosing explicit but arbitrary values for c and t, and determining the probability of parasites becoming extinct after this time, we instead assumed that a particular fraction of the hosts had become extinct. As described above, the probability that host j is extant at time t is qj ðtÞ, so the mean number of extant host species after time t is
SðtÞ ¼ 142
Y
X X ct qj ðtÞ ¼ e logðAj Þ ; j
particularly high or low extinction probabilities, given its number of hosts. To do this, bootstrap distributions of the extinction probabilities were generated by randomly resampling, with replacement, the geographic ranges Aj (and, hence, extinction rates r j ) of the host species. This allows testing of the null hypothesis that there is no association between host vulnerability and particular parasite species or groups. To assess the effect of host vulnerability on the extinction probabilities of the parasite species, the observed estimates were tested to confirm whether those had a significant tendency to be greater or smaller than the medians of the bootstrap confidence intervals (CIs), using a chi-square test. Differences amongst parasite taxonomic groups (Acanthocephala, Cestoda, Monogenea, Nematoda, Trematoda) were tested with a Fisher’s exact test. A re-sampling (permutation) process was used to compare the extinction probabilities amongst helminth taxonomic groups, and between species with direct and indirect life cycles. This was tested with a re-sampling ANOVA, where we considered different percentages of host species becoming extinct, and a nested relationship between helminth life cycle and taxonomic group. We did 1000 re-samplings, with replacement. Since information on the life cycle of anuran parasites is scarce, the literature was searched for each family and it was assumed that all helminths of a given family would have the same type of life cycle, i.e. direct or indirect. This analysis was conducted with 181 helminth species, because some species in the dataset are inquenda or insertae sedis and were removed. The data set comprised 157 anurans and 194 helminth species. The number of hosts to which a parasite is associated (parasite specificity from here on) was on average 3.7 (SD = 6.68); 52% of the helminth species were associated with a single host species. Monogenea were the most specialised parasites, while Nematoda were the most generalist (Table 1). Parasite species associated with few hosts had higher extinction probabilities (Fig. 1). The vulnerability of hosts associated with specialist (one host) parasites did not differ from other hosts (U = 2670, P = 0.5638). Notwithstanding, 75% of the extinction probabilities generated by the null model were higher than expected if the actual geographic range of each host species was considered (v2 = 45.55, degrees of freedom (df) = 1, P < 0.001). This indicates that most helminths depend on hosts with a higher than average vulnerability to extinction. However, 44% of the specialist parasites had significantly greater extinction probabilities (v2 = 6.01, df = 2, P = 0.049), with Monogenea being the parasite group most negatively affected by their hosts’ vulnerability (i.e. extinction probability was increased; Fisher’s Exact Test for Count Data P = 0.02). Forty-six percent of the helminth species reported have a direct life cycle. Hence, extinction probabilities varied amongst helminth species of different taxonomic groups and life cycle complexity (Fig. 2) with a significant interaction between these factors (Table 2). Therefore, the extinction probabilities tended to be
Table 1 Number of hosts reported in helminth species of different taxonomic groups of parasites from South American anurans.
j
Reported hosts 143 144 145 146 147 148 149 150 151
where the sum runs over all host species. Both qj ðtÞ and SðtÞ depend only on the product ct, so a non-linear equation solver can be used to numerically find the value of ct corresponding to a particular value of SðtÞ, and hence determine the parasite’s extinction probabilities at the point when a particular number of host extinctions have taken place. We used Mann–Whitney U tests to compare extinction rates between different parasite specificity groups (generalists and specialists). We also tested whether a parasites species had
Number of helminth species in each taxonomic group A
C
M
N
T
1 2 >2
2 0 3
6 1 1
10 1 0
58 14 33
35 12 18
Total
5
8
11
105
65
Mean of reported hosts (±S.D.)
3.4 ± 2.6
2.1 ± 2.61
1.1 ± 0.28
3.9 ± 7.53
2.2 ± 2.1
A, Acanthocephala; C, Cestoda; M, Monogenea; N, Nematoda; T, Trematoda.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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Fig. 1. Relation of parasite specificity (number of hosts) and extinction probability of helminth parasites of South American anurans. Lines represent different extinction scenarios that vary with the number of extant anuran species.
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higher in parasites with a direct life cycle, but this is probably because the most specialised parasites, i.e. the monogeneans, have a direct life cycle.
3
Our estimates confirmed specialist parasites as the most vulnerable to coextinction. Because parasites ultimately need their hosts for persistence, the number of host species a parasite is associated with is the most crucial parasite trait determining its risk of extinction (Moir et al., 2010). Hence, parasites that exploit different host species have the advantage of being less threatened by extinction, but this comes with the cost of overcoming the physiological and behavioural resistance of different hosts. Although this trade-off seems clear, the course to identify the extent of parasite specificity remains challenging. Many parasite species considered restricted to a narrow set of hosts might occur in other unsampled hosts, which leads to the overestimation of their extinction probabilities (see Brooks et al., 2006 for broader perspective on parasite specificity). On the other hand, extinction probability of generalist parasites may be underestimated by at least two means. First, our model assumes parasites exploited all host species equally, which is a simplification of what actually occurs. Generalist parasites may have a preferred host, whose extinction could affect parasite fitness in a way that would subsequently lead to its extinction (Streicker et al., 2013). Secondly, recent evidence has revealed that generalist parasite species may actually be subsets of cryptic specialists (Keeney et al., 2014; Selbach et al., 2015). Cryptic species are morphologically similar and can only be distinguished by molecular data (Bray and Cribb, 2015). These have been commonly found amongst parasites, because they often have large populations and undergo rapid evolution, which may favour cryptic speciation (Xavier et al., 2015). Thus, the fraction of generalist parasites in our data may comprise a subset of cryptic helminth diversity, since most reports did not include molecular investigations. This would imply
Fig. 2. Estimates of coextinction probabilities of helminth parasites of South American anurans. Letters represent helminth groups: A, Acanthocephala; C, Cestoda; M, Monogenea; N, Nematoda and T, Trematoda. Box plots indicate median lines, 25th and 75th percentiles, with whiskers denoting the 1.5 interquartile ranges and points indicating outliers.
Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010
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Table 2 Nested ANOVA comparing the effect of host species extinction amongst helminth species with direct and indirect life cycles, and the major taxonomic groups (Acanthocephala, Monogenea, Cestoda, Nematoda, Trematoda). Variables Extinct host species (%) Life cycle type (direct/indirect) Life cycle/helminth taxonomic group Residuals
Sum of squares
Mean squares
F value
Pa
1 1 3
63.86 0.18 1.17
63.86 0.18 0.39
1954.14 5.68 11.96
0.00 0.02 0.00
899
29.38
0.03
df
df, degrees of freedom. a P value was determined based on 1000 re-samplings.
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that with the higher coextinction probabilities for the species analysed here, and as mentioned by Dobson et al. (2008), a considerable fraction of helminth diversity may become extinct before being identified and classified. For most parasites, the chance of coextinction was decreased by additionally taking their host’s vulnerability to extinction into consideration (i.e. their geographic range). However, the effect was least marked amongst specialist parasites. Since host vulnerability in our null model is assigned at random from the empirical set of vulnerabilities, this suggests that generalist parasites depend on hosts that are more vulnerable than average, whereas specialist parasites do not. Indeed, we found that the vulnerabilities of hosts of specialist parasites were not significantly different from those of other hosts. A recent study on a global fish–parasite interaction network found that the most specialised species tended to occur in nonthreatened hosts, minimising their extinction risks (Strona et al., 2013). We found different results for anurans. Specialised parasites are as likely to occur in vulnerable hosts as are the generalists, being therefore the most prone to extinction. Powell (2011) found similar results in an insect–plant mutualist system, which did not support reduced specialisation of dependent species on the threatened hosts. Additionally, Powell (2011) observed that the densities of dependants in the threatened hosts were lower, suggesting they might become extinct earlier, as a response to lower abundance of a particular a host. Therefore, the extinction rates of parasite species could exceed the number of extinctions of free-living organisms, and parasites may become extinct more rapidly than their hosts (Koh et al., 2004; Dunn et al., 2009; Lafferty, 2012). This is of particular concern for amphibians, a vertebrate group with a high number of threatened species (threat stats available at http://www.iucnredlist.org/), implying that a considerable number of parasites might become extinct even before being discovered. Moreover, considering that helminth parasite diversity can contribute to a decrease in the disease risk in anurans (Johnson et al., 2013), the loss of parasite species could have unpredictable consequences in amphibian conservation and ecosystem health. The extinction probabilities in this analysis tended to be higher for parasites with direct life cycles, but this might not hold if their intermediate hosts were taken into account. Complex life-cycle parasites depend, additionally, on the persistence of their intermediate hosts, and could become extinct due to the lack of such hosts even if their definitive anuran host is not endangered (Lafferty, 2012). Nonetheless, it has been suggested that parasites are able to include, change, or even reduce the number of hosts required to complete their life cycle (Poulin and Cribb, 2002; Parker et al., 2003), which could potentially increase their chances of survival in a host extinction scenario. The variation in extinction probabilities between direct and indirect life cycles may be explained by the most specialised parasites having direct life cycles, eg the monogeneans. Thus, coextinction probabilities vary according to life cycle complexity and
are strongly influenced by parasite specificity, which in turn varies amongst taxonomic groups. This suggests that the coextinction probabilities for helminth parasites are phylogenetically constrained. In contrast, the hosts’ extinction probabilities might not be phylogenetically constrained. A study of the correlates of amphibian extinction risk revealed that the effect of phylogeny is weak, and geographic range is the best predictor (Sodhi et al., 2008). This suggests that in an anuran-helminth system, host vulnerability is mostly affected by extrinsic factors (i.e. habitat degradation), while the main driver of parasite risk is intrinsic (specificity). Overall, we found that the host specificity of parasites and the vulnerability of their hosts combine to determine the coextinction risks of anuran helminth parasites. They interact differently in different parasite taxonomic groups, and the most specialised groups are the most endangered.
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Acknowledgements
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We are grateful to Raul Costa Pereira for his help with data acquisition. K.M.C. and L.E.R.T. received fellowship grants from Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, Brazil) and Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPQ, Brazil), respectively.
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Please cite this article in press as: Campião, K.M., et al. Estimates of coextinction risk: how anuran parasites respond to the extinction of their hosts. Int. J. Parasitol. (2015), http://dx.doi.org/10.1016/j.ijpara.2015.08.010