- Email: [email protected]
Dwarf vs giant: An unexpected interaction between a small treefrog and a large nematode
Accepted Manuscript Dwarf vs giant: An unexpected interaction between a small treefrog and a large nematode
Karla M. Campião, Silionamã P. Dantas, Helane D. Tavares, Jucilla K.V. Martins, Fabrício H. Oda PII: DOI: Article Number: Reference:
S2352-2496(18)30025-9 doi:10.1016/j.fooweb.2018.e00102 e00102 FOOWEB 102
To appear in:
Food Webs
Received date: Revised date: Accepted date:
15 May 2018 9 October 2018 9 October 2018
Please cite this article as: Karla M. Campião, Silionamã P. Dantas, Helane D. Tavares, Jucilla K.V. Martins, Fabrício H. Oda , Dwarf vs giant: An unexpected interaction between a small treefrog and a large nematode. Fooweb (2018), doi:10.1016/j.fooweb.2018.e00102
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Short communication “Food Web Notes” Dwarf vs Giant: an unexpected interaction between a small treefrog and a large nematode
Karla M. Campiãoa*, Silionamã P. Dantasb, Helane D. Tavaresc, Jucilla K.V. Martinsb, Fabrício
Universidade Federal do Paraná, Departamento de Zoologia, Centro Politécnico, Jardim das
CR
a
IP
T
H. Odac
Américas, 81531-980, Curitiba, Paraná, Brazil
Universidade Federal do Tocantins, Escola de Medicina Veterinária e Zootecnia, Laboratório de
US
b
c
AN
Anatomia Animal, 77804-970, Araguaína, Tocantins, Brazil
Universidade Regional do Cariri, Departamento de Química Biológica, Laboratório de
ED
M
Zoologia, Rua Coronel Antônio Luiz 1161, Pimenta, 63105-000, Crato, Ceará, Brazil
*Corresponding adress: Universidade Federal do Paraná, Departamento de Zoologia, Centro
PT
Politécnico, Jardim das Américas, 81531-980, Curitiba, Paraná, Brazil. E-mail:
AC
CE
[email protected]
1
ACCEPTED MANUSCRIPT Abstract Parasitism is one of the most common strategies of resource exploitation in the planet, and the body size of the interacting species is a key factor to understanding the ecology and evolution of this trophic strategy. Here we report for the first time an unexpected interaction
T
between a large nematode species of Eustrongylides (162 mm) and an adult female of the dwarf
IP
treefrog Dendropsophus nanus (28 mm). Species of Eustrongylides have complex life cycles,
CR
and their transmission occurs through a series of trophic interactions. The first intermediate hosts are oligochaetes, which can be ingested by several species of fish and, occasionally, by
US
amphibians and reptiles. The parasite cycle is completed when these hosts are preyed on by
AN
birds. Anurans fill an important trophic position in terrestrial and aquatic ecosystems, acting as prey and predators for a wide variety of invertebrates and vertebrates. In this sense, parasites are
M
good indicators of food web links, and the occurrence of a parasite in a host may reflect
ED
interactions between the host and its prey and predators. One intriguing fact we observed is the large size achieved by the parasite in a such a small host, since larger parasites tend to be
PT
associated with larger hosts that provide more relaxed niche constraints. Our finding raises many
CE
questions on the frequency and outcomes of such interactions, pointing to the critical influence
AC
of parasite transmission in food webs.
Keywords: Anura, Dendropsophus nanus, Eustrongylides, parasite, trophic transmission, body size, predator-prey interactions
Despite being not very charismatic figures, parasitic organisms often attract much attention. This interest may be driven either by their medical importance, an intriguing
2
ACCEPTED MANUSCRIPT evolutionary history, or even some morbid curiosity. Parasitism is also one of the most common strategies of resource exploitation on the planet (Poulin and Mourand, 2000; Dobson et al., 2008). Such a strategy is, by definition, based on the dependence of one organism upon another. Indeed, the Latin etymology of the word relies on its intimacy (par = near) and its most common
T
way of resource consumption (site = food). Body size is a key factor in understanding the
IP
ecology and evolution of this trophic strategy. Although it is not a defining characteristic, one of
CR
the most well-accepted concepts in the study of parasites is that they are smaller than the hosts they inhabit (Lafferty and Kuris, 2002). This is because the evolution of their body size is
US
constrained by their host’s body size. This rule was proposed by Harrison, who suggested that
AN
larger hosts have larger parasites (Harvey and Keymer, 1991). The validity of Harrison’s rule has been demonstrated for a broad array of taxa, including nematodes (Morand et al., 1996).
M
Species of Eustrongylides are parasites of the gastrointestinal tract of piscivorous birds.
ED
These parasites have a complex life cycle, and their transmission occurs through a series of trophic interactions. Adult Eustrongylides release their eggs with the feces of the infected
PT
definitive hosts. Once in freshwater environment, the eggs are ingested by oligochaetes, which
CE
are the first intermediate hosts. Inside the oligochaetes, the newly hatched larvae develop into the second and third-larval stage. The fourth larval stage is reached when the invertebrate is ingested
AC
by planktivorous and benthivorous fishes, which are usually the second intermediate hosts. Amphibians and reptiles can also act as second intermediate or paratenic hosts. The cycle is completed when the second intermediate host is ingested by a piscivorous bird, where the fourthstage larva will achieve sexual maturity and release eggs to the environment (Anderson, 2000; Spalding and Forrester, 2008; Branciari et al., 2016). This system has some peculiarities; one is that Eustrongylides are found in migratory water birds that may spread parasite eggs, resulting in
3
ACCEPTED MANUSCRIPT wide geographic distribution ranges (e.g, from Brazil to New Zealand). Also, these parasites are of zoonotic concern, and eating raw or undercooked infected fish may cause a quite severe disease in humans (Xiong et al., 2009). During an anuran survey on 24 December 2017 in a temporary puddle within a pasture
T
area in the northeastern Brazilian Savanna, i.e., Cerrado (7°22’26” S, 46°36’40” W), we
IP
observed a large nematode leaving the ventral region of an adult female of the dwarf treefrog
CR
Dendropsophus nanus. The endoparasite probably decreased the corporal condition of the treefrog, which seemed to be weakened. The treefrog was thinner when compared with co-
US
specifics recorded in the same site and did not move when disturbed by our presence (Fig. 1).
AN
We collected the parasite specimen and brought it to the lab, where it was measured and identified. To our surprise, the parasite’s total length reached 162 mm, more than five times
M
longer than its host, which had a snout-vent length of 28 mm. Based on morphological
ED
characteristics we identified the parasite as a larval specimen of Eustrongylides. Because only nematodes in mature stages have morphological traits that allow species-level identification, we
CE
even if it is a new taxon.
PT
could not determine to which of the three valid species of Eustrongylides the larva belongs to, or
Eustrongylides larvae have been reported parasitizing medium and large-sized frogs such
AC
as Xenopus laevis, Rhinella marina, Leptodactylus latrans, Lithobates berlandieri, L. catesbeianus, L. dunni, L. megapoda, L. warszewitschii, Pelophylax ridibundus (Vicente et al., 1991; Goldberg and Bursey, 2002; Lezama and Sarabia, 2002; Kuperman et al., 2004; Bursey and Brooks, 2010; Yildirimhan et al., 2012; Melo et al., 2016). These anuran hosts range from 50 to 240 mm in length, while parasites are smaller than we report here, the largest record being of 120 mm (see Anderson 2000, and Lezama et al., 2012). The dwarf treefrog Dendropsophus
4
ACCEPTED MANUSCRIPT nanus (Boulenger, 1889) is a small-sized (males: 2 - 2.2 cm, females: 2.3 - 2.8 cm), arboreal, and nocturnal frog. It has a wide distribution range, including almost all South America, and can be found in many habitat types, such as forests and open areas, and also seems to adapt well to anthropogenic disturbance (Lopez et al., 2015). It breeds in temporary puddles and swamp areas,
T
where males call on the herbaceous vegetation at the edge of water bodies (Reichle et al., 2004).
IP
Other larval and adult nematode species have been reported parasitizing D. nanus, but all of
CR
them are smaller sized (see Campião et al., 2014; da Graça et al., 2017)
The aquatic larval stage of D. nanus was probably the key element causing the infection
US
by the Eustrongylides larva. Tadpoles of D. nanus are herbivorous feeders but occasionally prey
AN
on smaller aquatic invertebrates (Rossa-Feres et al., 2004; Schulze et al., 2015). The tadpole of the dwarf treefrog might have preyed upon an infected oligochaete, acquiring the third-stage
M
Eustrongylides larva (Anderson, 2000; Spalding and Forrester, 2008). Anurans fit an important
ED
trophic position in terrestrial and aquatic ecosystems because they are preys and predators to a wide variety of invertebrates and vertebrates (Toledo, 2005; Toledo et al., 2007). Therefore,
PT
anurans are good candidates to act as intermediate hosts for many parasite taxa (Imasuen et al.,
CE
2012). In this sense, parasites are good indicators of food web links, and the occurrence of a parasite in a host may reflect interactions between the host and its preys and predators (Dobson
AC
et al., 2008).
The dwarf treefrog is a good potential intermediate host due to its small body size and mild anti-predatory behavior (Toledo and Haddad, 2009), which may allow the contact with a wide array of predators. However, if on one hand the small body size makes it a good candidate to be an intermediate host, on the other it does not favor the acquisition of a wide range of parasite taxa (Campião et al., 2015). Therefore, our finding is also unexpected because the
5
ACCEPTED MANUSCRIPT endoparasite communities of amphibians have a nested pattern, with small sized anuran species harboring common generalist parasite species, and rare parasites such as Eustrongylides would be more easily found in hosts with larger body size (Campião et al., 2015). The most intriguing fact in the association is how this parasite could achieve such a large
T
size in such a small host. Other atypical cases can be observed in nature, such as the
IP
nematomorphs, which reach very large sizes inside small invertebrate and vertebrate hosts (e.g.,
CR
Schmidt-Rhaesa and Lalramliana, 2011; Looney et al., 2012; Şaşi and Gianetto, 2016), or even the various cestode species that parasitize vertebrates (Kahalil et al., 2994). The body length of
US
an organism is not a perfect surrogate, but it is a good proxy of its size and energetic exchange
AN
with the environment. When we think about the rules governing the abundance, distribution, and interaction among organisms, the allometric ones are the most pervasive in nature (Hechinger,
M
2013). The body size of an organism is strictly related to its energetic demands and fecundity.
ED
Thus, larger parasites tend to interact with larger hosts that provide more relaxed niche constraints (Poulin, 2007). On the other hand, the fact that small hosts harbor low parasite
PT
abundance might help explain how this parasite attained a large body size. Parasite growth is
CE
negatively correlated with abundance, and the absence of competitors might have contributed to greater host exploitation (Morand and Poulin, 2002).
AC
Our finding highlights that there are still many cryptic interactions to be discovered in the tropics. Moreover, it raises some questions, such as: how frequent might be the association between the dwarf treefrog and the Eustrongylides species? How does the parasite affect the antipredator response of the infected dwarf treefrog to favor the predation by the final hosts? How does this association impact the trophic links in the ecosystem? We expect to continue studying this system for answers. Additionally, laboratory experiments of this and other field-
6
ACCEPTED MANUSCRIPT based observations may contribute to improving our understanding of this unexpected hostparasite interaction.
Acknowledgments
T
Fabrício H. Oda receive postdoctoral fellowship from Fundação Cearense de Apoio ao
IP
Desenvolvimento Científico e Tecnológico – Funcap / Coordenação de Aperfeiçoamento
CR
Pessoal de Nível Superior – CAPES. We thank Craig Layman, and two anonymous reviewers
US
for their helpful comments and improvements of the manuscript.
AN
Competing interests
The authors declare that there are no competing interests. We also certify that the anuran species
M
reported in the study is not threatened, and all procedures were approved by the ethics committee
ED
of the institution where the study was conducted.
PT
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ACCEPTED MANUSCRIPT Schulze, A., Jansen, M., Köhler, G., 2015. Tadpole diversity of Bolivia's lowland anuran communities: molecular identification, morphological characterisation, and ecological assignment. Zootaxa 4016, 1-111. http://dx.doi.org/10.11646/zootaxa.4016.1.1. Spalding, M.G., Forrester, D.J., 2008. Eustrongylidosis, in Atkinson, C.T., Thomas, N.J., Hunter,
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Xiong, F., Wang, G.T., Wu, S.G., Nie, P., 2009. Development of Eustrongylides ignotus
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ACCEPTED MANUSCRIPT Figure caption Fig. 1A. Specimens of the dwarf treefrog Dendropsophus nanus observed in a Brazilian Savanna area. B. A giant specimen of Eustrongylides larva (total length: 162 mm) leaving the ventral region of an adult female of the dwarf treefrog (snout-vent length: 28 mm). Photos by Silionamã
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CE
PT
ED
M
AN
US
CR
IP
T
P. Dantas.
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Figure 1
Karla M. Campião, Silionamã P. Dantas, Helane D. Tavares, Jucilla K.V. Martins, Fabrício H. Oda PII: DOI: Article Number: Reference:
S2352-2496(18)30025-9 doi:10.1016/j.fooweb.2018.e00102 e00102 FOOWEB 102
To appear in:
Food Webs
Received date: Revised date: Accepted date:
15 May 2018 9 October 2018 9 October 2018
Please cite this article as: Karla M. Campião, Silionamã P. Dantas, Helane D. Tavares, Jucilla K.V. Martins, Fabrício H. Oda , Dwarf vs giant: An unexpected interaction between a small treefrog and a large nematode. Fooweb (2018), doi:10.1016/j.fooweb.2018.e00102
This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
ACCEPTED MANUSCRIPT Short communication “Food Web Notes” Dwarf vs Giant: an unexpected interaction between a small treefrog and a large nematode
Karla M. Campiãoa*, Silionamã P. Dantasb, Helane D. Tavaresc, Jucilla K.V. Martinsb, Fabrício
Universidade Federal do Paraná, Departamento de Zoologia, Centro Politécnico, Jardim das
CR
a
IP
T
H. Odac
Américas, 81531-980, Curitiba, Paraná, Brazil
Universidade Federal do Tocantins, Escola de Medicina Veterinária e Zootecnia, Laboratório de
US
b
c
AN
Anatomia Animal, 77804-970, Araguaína, Tocantins, Brazil
Universidade Regional do Cariri, Departamento de Química Biológica, Laboratório de
ED
M
Zoologia, Rua Coronel Antônio Luiz 1161, Pimenta, 63105-000, Crato, Ceará, Brazil
*Corresponding adress: Universidade Federal do Paraná, Departamento de Zoologia, Centro
PT
Politécnico, Jardim das Américas, 81531-980, Curitiba, Paraná, Brazil. E-mail:
AC
CE
[email protected]
1
ACCEPTED MANUSCRIPT Abstract Parasitism is one of the most common strategies of resource exploitation in the planet, and the body size of the interacting species is a key factor to understanding the ecology and evolution of this trophic strategy. Here we report for the first time an unexpected interaction
T
between a large nematode species of Eustrongylides (162 mm) and an adult female of the dwarf
IP
treefrog Dendropsophus nanus (28 mm). Species of Eustrongylides have complex life cycles,
CR
and their transmission occurs through a series of trophic interactions. The first intermediate hosts are oligochaetes, which can be ingested by several species of fish and, occasionally, by
US
amphibians and reptiles. The parasite cycle is completed when these hosts are preyed on by
AN
birds. Anurans fill an important trophic position in terrestrial and aquatic ecosystems, acting as prey and predators for a wide variety of invertebrates and vertebrates. In this sense, parasites are
M
good indicators of food web links, and the occurrence of a parasite in a host may reflect
ED
interactions between the host and its prey and predators. One intriguing fact we observed is the large size achieved by the parasite in a such a small host, since larger parasites tend to be
PT
associated with larger hosts that provide more relaxed niche constraints. Our finding raises many
CE
questions on the frequency and outcomes of such interactions, pointing to the critical influence
AC
of parasite transmission in food webs.
Keywords: Anura, Dendropsophus nanus, Eustrongylides, parasite, trophic transmission, body size, predator-prey interactions
Despite being not very charismatic figures, parasitic organisms often attract much attention. This interest may be driven either by their medical importance, an intriguing
2
ACCEPTED MANUSCRIPT evolutionary history, or even some morbid curiosity. Parasitism is also one of the most common strategies of resource exploitation on the planet (Poulin and Mourand, 2000; Dobson et al., 2008). Such a strategy is, by definition, based on the dependence of one organism upon another. Indeed, the Latin etymology of the word relies on its intimacy (par = near) and its most common
T
way of resource consumption (site = food). Body size is a key factor in understanding the
IP
ecology and evolution of this trophic strategy. Although it is not a defining characteristic, one of
CR
the most well-accepted concepts in the study of parasites is that they are smaller than the hosts they inhabit (Lafferty and Kuris, 2002). This is because the evolution of their body size is
US
constrained by their host’s body size. This rule was proposed by Harrison, who suggested that
AN
larger hosts have larger parasites (Harvey and Keymer, 1991). The validity of Harrison’s rule has been demonstrated for a broad array of taxa, including nematodes (Morand et al., 1996).
M
Species of Eustrongylides are parasites of the gastrointestinal tract of piscivorous birds.
ED
These parasites have a complex life cycle, and their transmission occurs through a series of trophic interactions. Adult Eustrongylides release their eggs with the feces of the infected
PT
definitive hosts. Once in freshwater environment, the eggs are ingested by oligochaetes, which
CE
are the first intermediate hosts. Inside the oligochaetes, the newly hatched larvae develop into the second and third-larval stage. The fourth larval stage is reached when the invertebrate is ingested
AC
by planktivorous and benthivorous fishes, which are usually the second intermediate hosts. Amphibians and reptiles can also act as second intermediate or paratenic hosts. The cycle is completed when the second intermediate host is ingested by a piscivorous bird, where the fourthstage larva will achieve sexual maturity and release eggs to the environment (Anderson, 2000; Spalding and Forrester, 2008; Branciari et al., 2016). This system has some peculiarities; one is that Eustrongylides are found in migratory water birds that may spread parasite eggs, resulting in
3
ACCEPTED MANUSCRIPT wide geographic distribution ranges (e.g, from Brazil to New Zealand). Also, these parasites are of zoonotic concern, and eating raw or undercooked infected fish may cause a quite severe disease in humans (Xiong et al., 2009). During an anuran survey on 24 December 2017 in a temporary puddle within a pasture
T
area in the northeastern Brazilian Savanna, i.e., Cerrado (7°22’26” S, 46°36’40” W), we
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observed a large nematode leaving the ventral region of an adult female of the dwarf treefrog
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Dendropsophus nanus. The endoparasite probably decreased the corporal condition of the treefrog, which seemed to be weakened. The treefrog was thinner when compared with co-
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specifics recorded in the same site and did not move when disturbed by our presence (Fig. 1).
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We collected the parasite specimen and brought it to the lab, where it was measured and identified. To our surprise, the parasite’s total length reached 162 mm, more than five times
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longer than its host, which had a snout-vent length of 28 mm. Based on morphological
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characteristics we identified the parasite as a larval specimen of Eustrongylides. Because only nematodes in mature stages have morphological traits that allow species-level identification, we
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even if it is a new taxon.
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could not determine to which of the three valid species of Eustrongylides the larva belongs to, or
Eustrongylides larvae have been reported parasitizing medium and large-sized frogs such
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as Xenopus laevis, Rhinella marina, Leptodactylus latrans, Lithobates berlandieri, L. catesbeianus, L. dunni, L. megapoda, L. warszewitschii, Pelophylax ridibundus (Vicente et al., 1991; Goldberg and Bursey, 2002; Lezama and Sarabia, 2002; Kuperman et al., 2004; Bursey and Brooks, 2010; Yildirimhan et al., 2012; Melo et al., 2016). These anuran hosts range from 50 to 240 mm in length, while parasites are smaller than we report here, the largest record being of 120 mm (see Anderson 2000, and Lezama et al., 2012). The dwarf treefrog Dendropsophus
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ACCEPTED MANUSCRIPT nanus (Boulenger, 1889) is a small-sized (males: 2 - 2.2 cm, females: 2.3 - 2.8 cm), arboreal, and nocturnal frog. It has a wide distribution range, including almost all South America, and can be found in many habitat types, such as forests and open areas, and also seems to adapt well to anthropogenic disturbance (Lopez et al., 2015). It breeds in temporary puddles and swamp areas,
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where males call on the herbaceous vegetation at the edge of water bodies (Reichle et al., 2004).
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Other larval and adult nematode species have been reported parasitizing D. nanus, but all of
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them are smaller sized (see Campião et al., 2014; da Graça et al., 2017)
The aquatic larval stage of D. nanus was probably the key element causing the infection
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by the Eustrongylides larva. Tadpoles of D. nanus are herbivorous feeders but occasionally prey
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on smaller aquatic invertebrates (Rossa-Feres et al., 2004; Schulze et al., 2015). The tadpole of the dwarf treefrog might have preyed upon an infected oligochaete, acquiring the third-stage
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Eustrongylides larva (Anderson, 2000; Spalding and Forrester, 2008). Anurans fit an important
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trophic position in terrestrial and aquatic ecosystems because they are preys and predators to a wide variety of invertebrates and vertebrates (Toledo, 2005; Toledo et al., 2007). Therefore,
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anurans are good candidates to act as intermediate hosts for many parasite taxa (Imasuen et al.,
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2012). In this sense, parasites are good indicators of food web links, and the occurrence of a parasite in a host may reflect interactions between the host and its preys and predators (Dobson
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et al., 2008).
The dwarf treefrog is a good potential intermediate host due to its small body size and mild anti-predatory behavior (Toledo and Haddad, 2009), which may allow the contact with a wide array of predators. However, if on one hand the small body size makes it a good candidate to be an intermediate host, on the other it does not favor the acquisition of a wide range of parasite taxa (Campião et al., 2015). Therefore, our finding is also unexpected because the
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ACCEPTED MANUSCRIPT endoparasite communities of amphibians have a nested pattern, with small sized anuran species harboring common generalist parasite species, and rare parasites such as Eustrongylides would be more easily found in hosts with larger body size (Campião et al., 2015). The most intriguing fact in the association is how this parasite could achieve such a large
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size in such a small host. Other atypical cases can be observed in nature, such as the
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nematomorphs, which reach very large sizes inside small invertebrate and vertebrate hosts (e.g.,
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Schmidt-Rhaesa and Lalramliana, 2011; Looney et al., 2012; Şaşi and Gianetto, 2016), or even the various cestode species that parasitize vertebrates (Kahalil et al., 2994). The body length of
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an organism is not a perfect surrogate, but it is a good proxy of its size and energetic exchange
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with the environment. When we think about the rules governing the abundance, distribution, and interaction among organisms, the allometric ones are the most pervasive in nature (Hechinger,
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2013). The body size of an organism is strictly related to its energetic demands and fecundity.
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Thus, larger parasites tend to interact with larger hosts that provide more relaxed niche constraints (Poulin, 2007). On the other hand, the fact that small hosts harbor low parasite
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abundance might help explain how this parasite attained a large body size. Parasite growth is
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negatively correlated with abundance, and the absence of competitors might have contributed to greater host exploitation (Morand and Poulin, 2002).
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Our finding highlights that there are still many cryptic interactions to be discovered in the tropics. Moreover, it raises some questions, such as: how frequent might be the association between the dwarf treefrog and the Eustrongylides species? How does the parasite affect the antipredator response of the infected dwarf treefrog to favor the predation by the final hosts? How does this association impact the trophic links in the ecosystem? We expect to continue studying this system for answers. Additionally, laboratory experiments of this and other field-
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ACCEPTED MANUSCRIPT based observations may contribute to improving our understanding of this unexpected hostparasite interaction.
Acknowledgments
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Fabrício H. Oda receive postdoctoral fellowship from Fundação Cearense de Apoio ao
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Desenvolvimento Científico e Tecnológico – Funcap / Coordenação de Aperfeiçoamento
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Pessoal de Nível Superior – CAPES. We thank Craig Layman, and two anonymous reviewers
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for their helpful comments and improvements of the manuscript.
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Competing interests
The authors declare that there are no competing interests. We also certify that the anuran species
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reported in the study is not threatened, and all procedures were approved by the ethics committee
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of the institution where the study was conducted.
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ACCEPTED MANUSCRIPT Figure caption Fig. 1A. Specimens of the dwarf treefrog Dendropsophus nanus observed in a Brazilian Savanna area. B. A giant specimen of Eustrongylides larva (total length: 162 mm) leaving the ventral region of an adult female of the dwarf treefrog (snout-vent length: 28 mm). Photos by Silionamã
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P. Dantas.
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Figure 1