Symbiosis

DOI 10.1007/s13199-017-0500-9

SHORT COMMUNICATION

Host bromeliads and their associated frog species:

Further considerations on the importance of species
interactions for conservation
Leandro Talione Sabagh 1 & Rodrigo Barbosa Ferreira 2 & Carlos Frederico Duarte Rocha 1

Received: 10 September 2016 / Accepted: 19 July 2017

# Springer Science+Business Media B.V. 2017

Abstract Bromeliads constitute a good example of symbiosis 1 Introduction

with organisms that spend their entire life cycle inside the
plants, and often depend on them to breed. The bromeliads In nature, one species can support the existence of another
benefit from this interaction by increasing their nutrients in- simply by providing a substrate on or in which the second
take. Conservation efforts tend to focus on a single endan- species can live, as in the case of the family Bromeliaceae
gered species, but in symbiotic associations, the viability of (Hastings et al. 2007). Bromeliads are one prominent example
one species depends on that of the other. Based on IUCN of an organism that supports many other forms of life (Rocha
criteria, any species that depends on another to complete its et al. 2000). The complex architecture of bromeliad anatomy
life cycle should be assigned a conservation status equivalent includes the spiral arrangement of the leaves, which form a
to that of the host taxon, where appropriate. We gathered pub- reservoir of water and accumulate leaf litter, providing micro-
lished plus fieldwork data on the frog-bromeliad mutualism habitats for a wide array of organisms in addition to resources
and compiled a checklist of 99 bromeligenous frogs species such as foraging sites, refuges from predators, and develop-
associated to 69 bromeliad hosts, and found threatened bro- ment sites. The collection and storage of water by tank bro-
meliads hosting non-threatened frogs. We found that 62% meliads is a prominent ecological phenomenon, and the stored
bromeligenous frogs inhabit unspecified bromeliads. Finally, water represents a vital resource for many micro- and macro-
we propose strategies for improving understanding and con- organisms, including invertebrates, vertebrates and even other
servation of the frog-bromeliad mutualism. plants. There is a high rate of endemism in the aquatic fauna of
bromeliads (Lopez et al. 2009), which underscores their im-
portance for conservation (Rocha et al. 2004).
Keywords Animal-plant interaction . Anura . Co-threatened The importance of bromeliads as sites for completion of life
species . Mutualism cycles of different organisms was first described a century ago
(Picado 1913). In some cases, the associative organisms are not
strictly dependent on the host bromeliad, but in others, the
Electronic supplementary material The online version of this article bromeliad tank hosts the development of the complete life cy-
(doi:10.1007/s13199-017-0500-9) contains supplementary material,
which is available to authorized users.
cle. A good example are the bromeligenous frogs (Peixoto
1995), species that spend their entire life cycle within the bro-
* Leandro Talione Sabagh meliad host. Bromeliad tanks are not merely aquaria, but living
[email protected] ecosystems that interact with the different organisms that inhab-
it them. In addition to the advantages for frogs, the bromeliad
1
benefits from the presence of these animals, for example by
Laboratório de Ecologia de Vertebrados, Universidade do Estado do
Rio de Janeiro, Rua São Francisco Xavier 524, Rio de
absorbing nitrogen from their feces (Romero et al. 2010).
Janeiro, RJ 20550-013, Brazil Bromeligenous frog species cannot live without their host bro-
2
Laboratório de Ecologia de Populações e Conservação,
meliad, and play an important role in the nutrition of the plant.
Pós-Graduação em Ecologia de Ecossistemas, Universidade Vila In recent years, the global decline in frog populations,
Velha, Vila Velha, ES 29102-920, Brazil caused primarily by habitat destruction, climate change and
 Sabagh L.T. et al.

diseases (especially chytridiomycosis) in highland areas between the conservation status of bromeligenous frogs and
(Young et al. 2001) are major conservation challenges. To date, their altitudinal distribution.
the relationships of bromeligenous frogs with their hosts has We tabulated all the data by frog species and, in addition,
received little attention. While conservation efforts are often compiled a single binary dataset with absence (0) or presence
directed primarily at single endangered species, the integration (1) of interaction between each frog and bromeliad species. To
of host or hosted species, and the rest of the community is visualise the structure of the associations between frog species
increasingly important. When the mutualism is obligatory, and their host bromeliads, we constructed a mutualistic net-
one species is not viable in the absence of the other (Koh work using the Pajek software (Mrvar and Batagelj 2012). For
et al. 2004). The International Union for Conservation of this network, we considered only records that identified both
Nature (IUCN) recommends that, if one species is dependent frog and bromeliad to the species level.
on another for all or part of its life cycle, it should be assigned a
conservation status equivalent to that of the host taxon, where
appropriate (IUCN 2012a). Based on this recommendation and 3 The host bromeliad is not known for many frog
of co-extinction (Stork and Lyal 1993), the conservation of a species
bromeligenous frog species cannot be achieved without the
conservation of its bromeliad host. We identified 99 bromeligenous frog species, which used 69
The available data on bromeliad-frog relationships have bromeliad species as breeding sites (Table 1). We built a mu-
until now been scattered in the literature, and there has been tualistic network where species were grouped top to bottom
no comprehensive review for their conservation. In the present by those that have the most symbionts. There were only 37
paper, we have compiled the available data and evaluated frog species for which host bromeliads were identified (Supp.
implications from a conservation perspective. Material 1). The host bromeliad of 62 bromeligenous frogs
was not known to species level (Fig. 1). Overall, 41% of the
frogs are listed as threatened, 23% as non-threatened, and the
2 Literature survey and data analysis status of 35% is assessed as unknown (see above).
We evaluated the altitudinal range of 77 bromeligenous
An extensive literature search, to compile records of frog species (Supp. Material 2) and found that all the frogs
bromeligenous frogs and their host bromeliads, was that typically occur at high altitudes (above 2000 m a.s.l.) are
conducted. We considered bromeligenous frogs as species currently classified as DD, NT or EN. Non-threatened species
that exclusively use bromeliads as breeding sites. Species were usually found below 1800 m a.s.l.
that use other types of breeding sites, even if they also are There are a number of important inconsistencies between
found with bromeliads, were not included. The conservation the conservation status of bromeligenous frogs and their host
status of bromeligenous frogs was based on the IUCN (2012b) bromeliads (Table. 1; Supplementary Material 1). For exam-
lists and on those suggested in national lists (Powell and ple, Osteocephalus planiceps (LC) has a wide geographic dis-
Incháustegui 2009; Barrio-Amorós and Torres 2010; Hedges tribution, being found in Brazil, Colombia, Ecuador and Peru,
and Díaz 2011; ICMBio 2014; Coloma et al. 2015). For bro- but only in its host, Aechmea zebrine. This bromeliad is EN in
meliads, we also used information in IUCN (2012b) and sug- Colombia but is non-threatened in others countries where it
gestions from national lists (Llamozas et al. 2003; García and hosts others Osteocephalus species and Pristimantis
Galeano 2006; Manzanares 2011; León et al. 2013; CNCFlora orphnotaimus (found in A. zebrina from Ecuador and Peru).
2016). When disagreements occurred between IUCN and na- More important examples are the non-threatened frog,
tional lists, we adopted the most restrictive category. We used Phyllodytes melanomystax, that has been found in one EN
the standard conservation categories: DD (Data Deficient); LC bromeliad host (Hohenbergia littoralis) and another NE spe-
(Least Concern); NT (Near Threatened); VU (Vulnerable); cies (Aechmea aquilega) from Brazilian Atlantic Forest. By
EN (Endangered); CR (Critically Endangered); and NE (Not contrast, Ololygon littorea and O. perpusilla, both non-
Evaluated). New and undescribed species (aff. and gr. species) threatened treefrogs from the Brazilian Atlantic Forest, inhabit
were classified as NE. For the analysis, we considered NE + a number of non-threatened bromeliads, but they are found
DD as Bunknown status^, CR + EN + VU + NT as primarily in a threatened (EN) bromeliad species Alcantarea
Bthreatened^, and LC as Bnon-threatened^. glaziouana. Another complexity in the Brazilian Atlantic
We quantified the number of bromeliad species used by the Forest is the VU classification of the frog Adelophryne
frogs and defined the number of host bromeliads used by each maranguapensis, as two of its four host bromeliads
frog. To avoid overestimates, we counted genera only once (Guzmania sanguinea and Vriesea cearensis) are EN, and
when a congeneric species had already been identified, unless the others are either VU (G. lingulata) or NE (Aechmea
the congeneric had been identified by the same authority. We pernambucentris). Based on the IUCN criterion, this frog
also analysed the available data for a possible relationship should be assessed in a more restrictive EN category. All the
Table 1 List of bromeligenous frog species, threat category, host bromeliads, altitudinal range, and source

Frogs IUCN Bromeliad host Altitudinal Source

category distribution
(m a.s.l.)

Aromobatidae
Allobates bromelicola DD Unidentified 1300 Dixon and Rivero-Blanco 1985, Frost 2016
Anomaloglossus beebei VU Brocchinia micranta 450 Bourne et al. 2001, Kok et al. 2006, Frost 2016
Anomaloglossus Roraima DD Brocchinia tatei 1860–2700 Grant et al. 2006, Kok et al. 2013, Frost 2016
Brachycephalidae
Ischnocnema nasuta LC Unidentified 50–1300 Heyer 1984, Peixoto 1995
Ischnocnema venancioi LC Unidentified 800–1200 Lutz 1958, Peixoto 1995
Bufonidae
Dendrophryniscus berthalutzae LC Nidularrium innocentii; Vriesea incurvata 80–1100 Izecksohn 1993, Peixoto 1995, Fusinatto et al. 2008, Per. Obs.
Dendrophryniscus LC Neoregelia sp. < 900 Izecksohn 1993, Peixoto 1995, Fusinatto et al. 2008, Per. Obs.
brevipollicatus
Dendrophryniscus carvalhoi EN Vriesea simplex 800–1135 Izecksohn 1993, Peixoto 1995, Cassimiro and Rodrigues 2008
Dendrophryniscus krausae DD Unidentified 800–870 Cruz and Fusinatto 2008
Dendrophryniscus oreites* DD Unidentified 850 Recoder et al. 2010
Dendrophryniscus organensis* DD Unidentified 1050 Carvalho-e-Silva et al. 2010
Dendrophryniscus stawiarskyi DD Unidentified 980 Izecksohn 1993, Peixoto 1995
Frostius erythrophthalmus* DD Unidentified 140–920 Pimenta and Caramaschi 2007
Frostius pernambucensis LC Vriesea noblickii; Nidularium sp. < 800 Cruz and Peixoto 1982, Peixoto 1995, Juncá and Borges 2002, Juncá 2006
Melanophryniscus alipioi DD Vriesea platynema; Aechmea ornata > 1400 Langone et al. 2008, Crivellari et al. 2014
Melanophryniscus milanoi DD** Vriesea platynema; V. incurvata; Nidularium amazonicum 655–850 Bornschein et al. 2015
(= Wittrockia smithii); N. procerum
Melanophryniscus DD** Aechmea distichantha; A. gamosepala; Vriesea incurvata; 565–1275 Bornschein et al. 2015
xanthostomus V. Philippocoburgi
Cycloramphidae
Crossodactylodes bokermanni NT Vriesea morreni 800–1477 Peixoto 1982, Frost 2016, Per. Obs.
Crossodactylodes itambe DD Vriesea medusa 1836–2062 Barata et al. 2013, Santos et al. 2017
Crossodactylodes izecksohni NT Aechmea capixabae; Aechmea lamarchei; Edmundoa 650–933 Peixoto 1982, Peixoto 1995, Pertel et al. 2006, Per. Obs.
lindenii; Neoregelia guttata; N. macrosepala;
N. pauciflora; Nidularium cariacicaensis;
Vriesea aff. atra; V. bituminosa; V. ensiformis; V. gracilior;
V. vagans
Crossodactylodes pintoi DD Unidentified 1200 Peixoto 1982, Peixoto 1995
Crossodactylodes NE Unidentified > 930 Teixeira et al. 2013
septentrionalis
Dendrobatidae
Ameerega andina DD Unidentified 1700–2020 Myers and Burrowes 1987, Frost 2016
Andinobates daleswansoni VU Unidentified 1800–2000 Rueda-Almonacid et al. 2006, Brown et al. 2011
Host bromeliads and their associated frog species: Further considerations on the importance of species interactions...

Andinobates dorisswansoni* CR Unidentified 1780 Rueda-Almonacid et al. 2006, Brown et al. 2011
Andinobates minutus LC Unidentified < 1000 Summers and McKeon 2004, Brown et al. 2011
Andinobates opisthomelas VU Unidentified 1160–2200 Myers and Daly 1980, Brown et al. 2011
Andinobates viridis VU Unidentified 100–1200 Castro-Herrera and Bolívar-García 2010, Brown et al. 2011
Excidobates mysteriosus EN Aechmea nudicaulis 950–1250 Lehtinen et al. 2004, Summers and McKeon 2004, Dendrobates.org 2016
Excidobates condor NE Guzmania sp. 1770–1930 Almendáriz et al. 2012
Oophaga arborea EN Unidentified < 1120 Lehtinen et al. 2004, Summers and McKeon 2004
Oophaga lehmanni CR Unidentified 600–1200 Lehtinen et al. 2004, Summers and McKeon 2004
Oophaga speciosa EN Unidentified 1140–1410 Summers et al. 1999
Andinobates abditus CR Unidentified 1700 Myers and Daly 1980, Brown et al. 2011
Ranitomeya amazonica* DD Pitcairnia geykessi; Aechmea aquilega; Catopsis berteroniana < 200 Brown et al. 2011
Andinobates bombetes EN Unidentified 1580–2100 Myers and Daly 1980
Ranitomeya defleri LC** Unidentified 68–260 Twomey and Brown 2009, Brown et al. 2011
Ranitomeya yavaricola NE Unidentified 120 Perez-Peña et al. 2010, Brown et al. 2011
Table 1 (continued)

Frogs IUCN Bromeliad host Altitudinal Source

category distribution
(m a.s.l.)

Eleutherodactylidae
Adelophryne mucronatus* NE Unidentified 79–126 Lourenco-De-Moraes et al. 2012
Adelophryne maranguapensis VU Guzmania lingulata; G. sanguinea; Vriesea cearensis; Aechmea pernambucentris 800–900 Cassiano-Lima et al. 2011
Eleutherodactylus gryllus EN Unidentified 300–1182 Joglar 1998, Hedges and Rios-López 2008
Eleutherodactylus jasperi CR Vriesea sp., Hohenbergia sp., Guzmania sp. 650–850 Drewry and Jones 1976, Joglar 1998
Eleutherodactylus VU Tillandsia sp. 60–1150 Hedges et al. 1992
guantanamera
Eleutherodactylus lamprotes CR Unidentified 818–1455 Hedges and Thomas 2004
Eleutherodactylus melacara EN Unidentified 840–1974 Hedges et al. 1992
Eleutherodactylus varians VU Tillandsia utriculata; Hohenbergia penduliflora 0–845 García-González et al. 2014
Hemiphractidae
Fritziana fissilis LC Nidularium sp.; Bilbergia sp.; Vriesea bituminosa; Racinaea spiculosa; Aechmea 500–1800 Duellman and Maness 1980, Pertel et al. 2006, Heyer et al. 1990, Frost 2016, Per.
lindenii Obs.
Fritziana aff. fissilis Vriesea platynema 448–850 Franz and Mello 2015
Fritziana goeldii LC Alcantarea imperialis; Aechmaea nudicaulis; 430–1220 Lutz 1954, Duellman and Maness 1980, Peixoto 1995, Frost 2016, Per. Obs.
Aechmea lamarchei; Vriesea aff. a tra
Fritziana ulei NE Unidentified 500–1300 Folly et al. 2014
Gastrotheca fissipes LC Aechmea blanchetiana 76–700 Schineider and Teixeira 2001, Xavier and Dias 2015, Frost 2016
Gastrotheca ochoai DD Unidentified 2745–3080 Duellman 1979, Ângulo et al. 2004, Frost 2016
Hylidae
Aparasphenodon arapapa NT Aechmea gr. lingulata; A. blanchetiana; Araeococcus sp. 20–100 Pimenta et al. 2009, Lantyer-Silva et al. 2014, Lantyer-Silva A. (per. Comm.)
Bromeliohyla bromeliacia LC Unidentified 350–1790 Duellman 1970, Altig and McDiarmid 1999, Frost 2016
Bromeliohyla dendroscarta CR Unidentified 450–1900 Duellman 1970, Altig and McDiarmid 1999, Frost 2016
Dendropsophus bromeliaceus DD** Aechmea capixabae; Aechmea lamarchei; Aechmea pineliana; 745–922 Ferreira et al. 2015
Alcantarea extensa; Neoregelia pauciflora; Racinaeae
spiculosa; Vriesea bituminosa; Vriesea morrenii;
Vriesea ruschii; Vriesea aff. Atra; Vriesea ensiformis;
Vriesea vagans; Nidularium cariacicaense; Nidularium
espiritosantensis; Nidularium sp.
Isthmohyla melacaena NT Unidentified 1370–1990 McCranie and Castaneda 2006, Frost 2016
Isthmohyla picadoi NT Unidentified 1900–2650 Dunn 1937, Duellman 1970, Lips 1998, Savage 2002, Stuckert et al. 2009, Frost 2016
Isthmohyla zetecki NT Unidentified 1200–1804 Dunn 1937, Duellman 1970, Savage 2002, Frost 2016
Osteocephalus deridens LC Aechmea zebrina; A. chantinii 250–600 Jungfer et al. 2000, Lehtinen et al. 2004, Frost 2016
Osteocephalus fuscifacies DD Aechmea zebrina 250–600 Jungfer et al. 2000, McCracken and Forstner 2014, Frost 2016
Tepuihyla exophthalma DD Brocchinia sp. 585–1550 Smith and Noonan 2001, MacCulloch and Lathrop 2005, Frost 2016
Osteocephalus planiceps LC Aechmea zebrina 200–700 Guayasamin et al. 2006, McCracken and Forstner 2006, 2008, 2014, Frost 2016
Osteopilus crucialis EN Hohenbergia urbiana 0–1200 Garrick et al. 1985, Hedges 1987, Frost 2016
Osteopilus marianae EN Tillandsia sp. 120–880 Hedges 1987, Frost 2016
Osteopilus ocellatus LC Tillandsia deppeana; Hohenbergia fawcettii 0–1500 Laessle 1961, Lannoo et al. 1987, Frost 2016
Osteopilus wilderi EN Tailândia sp. 120–880 Laessle 1961, Hedges 1987, Crombie 1999, Frost 2016
Phyllodytes acuminatus LC Encholirium spectabile; Aechmea leptantha 863 Caramaschi and Peixoto 2004, Peixoto and Pimenta 2004, Campos et al. 2014, Frost
2016
Phyllodytes brevirostris NT Aechmea patentíssima 0–30 Peixoto and Cruz 1988, Vieira et al. 2009, Frost 2016
Phyllodytes edelmoi NT Portea leptantha 0 Peixoto et al. 2003, Frost 2016, Ruano-Farjado et al. 2016
Phyllodytes gyrinaethes CR Unidentified 0–650 Peixoto et al. 2003, Frost 2016
Phyllodytes kautskyi LC Aechmea nudicaulis; A. blanchetiana; A. phanerophlebia; 22–650 Peixoto and Cruz 1988, Simon and Gasparini 2003, Simon and
A. chlorophyla Peres 2012
Phyllodytes luteolus LC Aechmea blanchetiana; A. nudicaulis; A. saxicola; 0–650 Teixeira et al. 1997, Eterovick 1999, Papp and Papp 2000, Schineider and
A. victoriana; Vrisea procera; Teixeira 2001,
V. neoglutinosa; Alcantaraea extensa; Hohenbergia Juncá and Borges 2002, Frost 2016
augusta; Quesnelia quesneliana
Sabagh L.T. et al.
Table 1 (continued)

Frogs IUCN Bromeliad host Altitudinal Source

category distribution
(m a.s.l.)

Phyllodytes melanomystax LC Hohenbergia littoralis; Aechmea aquilega 0–10 Caramaschi et al. 1992, Juncá 2006, Frost 2016, Cunha and Napoli 2016
Phyllodytes punctatus DD Hohenbergia sp. 0–10 Caramaschi and Peixoto 2004, Caldas et al. 2011, Frost 2016
Phyllodytes tuberculosus DD Unidentified 997 Caramaschi and Peixoto 2004, Caramaschi et al. 2004, Frost 2016
Phyllodytes wuchereri DD Unidentified 0–815 Caramaschi et al. 2004, Magalhães et al. 2015, Frost 2016
Phytotriades auratus CR Glomeropitcairnia erectiflora 940–1250 Hardy 2004, Hailey and Cazabon-Mannette 2011, Rivas and Freitas 2015
Ololygon alcatraz CR Unidentified 0–180 Duellman and Wiens 1992, Peixoto 1995
Ololygon arduoa DD Alcantarea sp.; Vriesea ruschii; Vriesea bituminosa; V. morrenii; 654–921 Pertel et al. 2010, Lacerda et al. 2015
V. vagans; V. aff. a tra; Quesnelia quesneliana
Ololygon atrata DD Unidentified 1200–1300 Peixoto 1988
Ololygon belloni EN Alcantarea sp. 600–1500 Faivovich et al. 2010
Ololygon cosenzai NE Alcantarea extensa 980–1385 Lacerda et al. 2012, Guimaraes et al. 2014
Ololygon faivovichi CR Unidentified 20–80 Brasileiro et al. 2007
Ololygon insperata DD Alcantarea imperialis; A. regina; Vriesea gigantea 680–845 Silva and Alves-Silva 2011
Ololygon littorea LC Alcantarea glauziouana; Neoregelia cruenta; Vriesea neoglutinosa 0–400 Alves-Silva and Silva 2009, Silva et al. 2011, Per. Obs
Ololygon melloi DD Alcatarea imperialis 1100–1215 Peixoto 1988, Per. Obs.
Ololygon peixotoi CR Unidentified 50 Brasileiro et al. 2007
Ololygon perpusilla LC Nidularium innocentii; Vriese a spp.; Aechmea spp.; 0–220 Peixoto 1987, Silva et al. 1988, Oliveira and Navas 2004, Teixeira et al. 2006,
Neoregelia cruenta; Alcantarea glauziouiana Alves-Silva and Silva 2009, Per. Obs.
Ololygon tupinambá NE Unidentified 20–344 Silva and Alves-Silva 2008
Ololygon v-signata LC Alcantarea imperialis; A. geniculata; Billbergia pyramidalis; 450–1220 Peixoto 1987, Per. Obs.
Edmundoa lindenii; Neoregelia concentrica; Vrisea inflata;
V. philippocoburgii.
Microhylidae
Ctenophryne carpish EN Unidentified 2750–2960 Lehr and Trueb 2007, Lehr et al. 2007, Frost 2016
Chiasmocleis antenori LC Guzmania weberbaueri 800–1500 Krügel and Richter 1995, Frost 2016
Strabomantidae
Pristimantis acuminatus LC Unidentified 100–1124 Rivero 1987, Rodríguez and Duellman 1994
Pristimantis aureolineatus NT Unidentified 190–350 Castro-Herrera and Bolívar-García 2010
Pristimantis buckleyi NT Unidentified 2400–3700 Lynch and Ruíz-Carranza 1985
Pristimantis celator NT Unidentified 1750–2800 Venegas 2007
Pristimantis orphnolaimus* DD Aechmea zebrina 250–350 Guayasamin et al. 2006, McCracken and Forstner 2006, 2008, 2014
Pristimantis wagteri* DD Unidentified 340–2456 Venegas 2007

* frogs species probably bromeligenous (according some authors and life history) but their reproduction mode is still unknown,
** IUCN category suggest by species author
Host bromeliads and their associated frog species: Further considerations on the importance of species interactions...
 Sabagh L.T. et al.

detected cases of a strong inconsistency are from the Brazilian large number of bromeliad species, apparently either because
Atlantic Rainforest. This biome is a conservation hotspot the frogs have been relatively well studied and/or because they
(Myers et al. 2000) and one of the most important centres of have a comparatively large geographic range (e.g. Phyllodytes
diversity and endemism for both frogs (Haddad et al. 2013) luteolus). Even so, the evidence indicates that bromeligenous
and bromeliads (Martinelli et al. 2008). frogs are selective. They seek specific characteristics, such as
The host bromeliads were not identified to species level for the size of the bromeliad tank, water quality in the
62% of the frogs species. Of these frogs, 52% were classified phytotelmata, or bromeliad identity. In other words, the frogs
as threatened, 11% as non-threatened, and 37% as having do not occupy bromeliads randomly (Eterovick 1999; Oliveira
unknown status (see Table 1). In some cases, the host brome- and Navas 2004; Mageski et al. 2015). For example,
liad was identified to genus. The high number of unidentified Ferreira et al. (2015) did not find Dendropsophus
bromeliads for the majority bromeligenous frog species con- bromeliaceus in all of the 11 bromeliad species available
trasts with the fact that some species of frogs have many as potential breeding sites. As co-extinction rates are
identified bromeliads hosts (Fig. 2). Only seven frog species known to depend on the number of partners (Koh et al.
have more than five species of bromeliad host. These species 2004), the more selective a frog is for its breeding sites,
(Ololygon arduoa, O. perpusilla, O. v-signata, Phyllodytes the more likely it is to be threatened by the loss of the
luteolus, Crossadactylodes izecksohni, Fritziana fissilis and selected bromeliad species.
Dendropsophus bromeliaceus - see also Table 1) were studied The status of bromeligenous frogs should be assessed based
by at least one of the authors of the present paper, herpetolo- on the conservation status of its host bromeliads. If the frog
gists with great interest in frog-bromeliad association. breeds in a single bromeliad species and this bromeliad is
Most frogs use just a few bromeliad species as breeding threatened, the frog must also be categorised as threatened.
sites. Only few frog species have been found to breed in a The more species of bromeliad hosts used, the lower the

Fig. 1 Star network of the 57 bromeligenous frogs with unidentified host bromeliads and their categories of threat. * = frogs species probably
bromeligenous (according to some authors and life history) but their reproduction mode are still unknown
Host bromeliads and their associated frog species: Further considerations on the importance of species interactions...

conserve these unique relationships and guarantee the conti-

nuity of this fascinating ecosystem.

Acknowledgements This study was supported by research grants from

Conselho Nacional de Desenvolvimento Científico e Tecnológico
(304791/2010-5; 470265/2010-8; 302974/2015-6; 161428/2015-0),
Fundação de Amparo à Pesquisa do Estado do Rio de Janeiro through
BCientistas do Nosso Estado^ (E-26/102.765/2012 and E-26/202.920/
2015) and Coordenação de Aperfeiçoamento de Pessoal de Nível
Superior/Fundação de Amparo à Pesquisa e Inovação do Espírito Santo.
We thank Dr. Néstor García for giving information about Colombian
bromeliads. We also thank Stuart Pimm and Bill Magnusson for their
suggestions in a draft version of this manuscript.

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