Host bromeliads and their associated frog species: Further considerations on the importance of species interactions for conservation

Abstract

Bromeliads constitute a good example of symbiosis with organisms that spend their entire life cycle inside the plants, and often depend on them to breed. The bromeliads benefit from this interaction by increasing their nutrients intake. Conservation efforts tend to focus on a single endangered species, but in symbiotic associations, the viability of one species depends on that of the other. Based on IUCN criteria, any species that depends on another to complete its life cycle should be assigned a conservation status equivalent to that of the host taxon, where appropriate. We gathered published plus fieldwork data on the frog-bromeliad mutualism and compiled a checklist of 99 bromeligenous frogs species associated to 69 bromeliad hosts, and found threatened bromeliads hosting non-threatened frogs. We found that 62% bromeligenous frogs inhabit unspecified bromeliads. Finally, we propose strategies for improving understanding and conservation of the frog-bromeliad mutualism.

Full text

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 / Published online: 16 August 2017
#Springer Science+Business Media B.V. 2017
Abstract Bromeliads constitute a good example of symbiosis
with organisms that spend their entire life cycle inside the
plants, and often depend on them to breed. The bromeliads
benefit from this interaction by increasing their nutrients in-
take. Conservation efforts tend to focus on a single endan-
gered species, but in symbiotic associations, the viability of
one species depends on that of the other. Based on IUCN
criteria, any species that depends on another to complete its
life cycle should be assigned a conservation status equivalent
to that of the host taxon, where appropriate. We gathered pub-
lished plus fieldwork data on the frog-bromeliad mutualism
and compiled a checklist of 99 bromeligenous frogs species
associated to 69 bromeliad hosts, and found threatened bro-
meliads hosting non-threatened frogs. We found that 62%
bromeligenous frogs inhabit unspecified bromeliads. Finally,
we propose strategies for improving understanding and con-
servation of the frog-bromeliad mutualism.
Keywords Animal-plant interaction .Anura .Co-threatened
species .Mutualism
1 Introduction
In nature, one species can support the existence of another
simply by providing a substrate on or in which the second
species can live, as in the case of the family Bromeliaceae
(Hastings et al. 2007). Bromeliads are one prominent example
of an organism that supports many other forms of life (Rocha
et al. 2000). The complex architecture of bromeliad anatomy
includes the spiral arrangement of the leaves, which form a
reservoir of water and accumulate leaf litter, providing micro-
habitats for a wide array of organisms in addition to resources
such as foraging sites, refuges from predators, and develop-
ment sites. The collection and storage of water by tank bro-
meliads is a prominent ecological phenomenon, and the stored
water represents a vital resource for many micro- and macro-
organisms, including invertebrates, vertebrates and even other
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).
The importance of bromeliads as sites for completion of life
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
bromeliad tank hosts the development of the complete life cy-
cle. A good example are the bromeligenous frogs (Peixoto
1995), species that spend their entire life cycle within the bro-
meliad host. Bromeliad tanks are not merely aquaria, but living
ecosystems that interact with the different organisms that inhab-
it them. In addition to the advantages for frogs, the bromeliad
benefits from the presence of these animals, for example by
absorbing nitrogen from their feces (Romero et al. 2010).
Bromeligenous frog species cannot live without their host bro-
meliad, and play an important role in the nutrition of the plant.
In recent years, the global decline in frog populations,
caused primarily by habitat destruction, climate change and
Electronic supplementary material The online version of this article
(doi:10.1007/s13199-017-0500-9) contains supplementary material,
which is available to authorized users.
*Leandro Talione Sabagh
leandro.sabagh@gmail.com
1
Laboratório de Ecologia de Vertebrados, Universidade do Estado do
Rio de Janeiro, Rua São Francisco Xavier 524, Rio de
Janeiro, RJ 20550-013, Brazil
2
Laboratório de Ecologia de Populações e Conservação,
Pós-Graduação em Ecologia de Ecossistemas, Universidade Vila
Velha, Vila Velha, ES 29102-920, Brazil
Symbiosis (2017) 73:201–211
DOI 10.1007/s13199-017-0500-9

diseases (especially chytridiomycosis) in highland areas
(Young et al. 2001) are major conservation challenges. To date,
the relationships of bromeligenous frogs with their hosts has
received little attention. While conservation efforts are often
directed primarily at single endangered species, the integration
of host or hosted species, and the rest of the community is
increasingly important. When the mutualism is obligatory,
one species is not viable in the absence of the other (Koh
et al. 2004). The International Union for Conservation of
Nature (IUCN) recommends that, if one species is dependent
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
of co-extinction (Stork and Lyal 1993), the conservation of a
bromeligenous frog species cannot be achieved without the
conservation of its bromeliad host.
The available data on bromeliad-frog relationships have
until now been scattered in the literature, and there has been
no comprehensive review for their conservation. In the present
paper, we have compiled the available data and evaluated
implications from a conservation perspective.
2 Literature survey and data analysis
An extensive literature search, to compile records of
bromeligenous frogs and their host bromeliads, was
conducted. We considered bromeligenous frogs as species
that exclusively use bromeliads as breeding sites. Species
that use other types of breeding sites, even if they also are
found with bromeliads, were not included. The conservation
status of bromeligenous frogs was based on the IUCN (2012b)
lists and on those suggested in national lists (Powell and
Incháustegui 2009; Barrio-Amorós and Torres 2010;Hedges
and Díaz 2011;ICMBio2014;Colomaetal.2015). For bro-
meliads, we also used information in IUCN (2012b) and sug-
gestions from national lists (Llamozas et al. 2003;Garcíaand
Galeano 2006;Manzanares2011;Leónetal.2013; CNCFlora
2016). When disagreements occurred between IUCN and na-
tional lists, we adopted the most restrictive category. We used
the standard conservation categories: DD (Data Deficient); LC
(Least Concern); NT (Near Threatened); VU (Vulnerable);
EN (Endangered); CR (Critically Endangered); and NE (Not
Evaluated). New and undescribed species (aff. and gr. species)
were classified as NE. For the analysis, we considered NE +
DD as Bunknown status^,CR+EN+VU+NTas
Bthreatened^,andLCasBnon-threatened^.
We quantified the number of bromeliad species used by the
frogs and defined the number of host bromeliadsused by each
frog. To avoid overestimates, we counted genera only once
when a congeneric species had already been identified, unless
the congeneric had been identified by the same authority. We
also analysed the available data for a possible relationship
between the conservation status of bromeligenous frogs and
their altitudinal distribution.
We tabulated all the data by frog species and, in addition,
compiled a single binary dataset with absence (0) or presence
(1) of interaction between each frog and bromeliad species. To
visualise the structure of the associations between frog species
and their host bromeliads, we constructed a mutualistic net-
work using the Pajek software (Mrvar and Batagelj 2012). For
this network, we considered only records that identified both
frog and bromeliad to the species level.
3 The host bromeliad is not known for many frog
species
We identified 99 bromeligenous frog species, which used 69
bromeliad species as breeding sites (Table 1). We built a mu-
tualistic network where species were grouped top to bottom
by those that have the most symbionts. There were only 37
frog species for which host bromeliads were identified (Supp.
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
status of 35% is assessed as unknown (see above).
We evaluated the altitudinal range of 77 bromeligenous
frog species (Supp. Material 2) and found that all the frogs
that typically occur at high altitudes (above 2000 m a.s.l.) are
currently classified as DD, NTor EN. Non-threatened species
were usually found below 1800 m a.s.l.
There are a number of important inconsistencies between
the conservation status of bromeligenous frogs and their host
bromeliads (Table. 1; Supplementary Material 1). For exam-
ple, Osteocephalus planiceps (LC) has a wide geographic dis-
tribution, being found in Brazil, Colombia, Ecuador and Peru,
but only in its host, Aechmea zebrine. This bromeliad is EN in
Colombia but is non-threatened in others countries where it
hosts others Osteocephalus species and Pristimantis
orphnotaimus (found in A. zebrina from Ecuador and Peru).
More important examples are the non-threatened frog,
Phyllodytes melanomystax, that has been found in one EN
bromeliad host (Hohenbergia littoralis) and another NE spe-
cies (Aechmea aquilega) from Brazilian Atlantic Forest. By
contrast, Ololygon littorea and O. perpusilla, both non-
threatenedtreefrogs from the Brazilian Atlantic Forest, inhabit
a number of non-threatened bromeliads, but they are found
primarily in a threatened (EN) bromeliad species Alcantarea
glaziouana. Another complexity in the Brazilian Atlantic
Forest is the VU classification of the frog Adelophryne
maranguapensis, as two of its four host bromeliads
(Guzmania sanguinea and Vriesea cearensis) are EN, and
the others are either VU (G. lingulata)orNE(Aechmea
pernambucentris). Based on the IUCN criterion, this frog
should be assessed in a more restrictive EN category. All the
202 Sabagh L.T. et al.

Tab l e 1 List of bromeligenous frog species, threat category, host bromeliads, altitudinal range, and source
Frogs IUCN
category
Bromeliad host Altitudinal
distribution
(m a.s.l.)
Source
Aromobatidae
Allobates bromelicola DD Unidentified 1300 Dixon and Rivero-Blanco 1985,Frost2016
Anomaloglossus beebei VU Brocchinia micranta 450 Bourne et al. 2001, Kok et al. 2006,Frost2016
Anomaloglossus Roraima DD Brocchinia tatei 1860–2700 Grant et al. 2006, Kok et al. 2013,Frost2016
Brachycephalidae
Ischnocnema nasuta LC Unidentified 50–1300 Heyer 1984,Peixoto1995
Ischnocnema venancioi LC Unidentified 800–1200 Lutz 1958,Peixoto1995
Bufonidae
Dendrophryniscus berthalutzae LC Nidularrium innocentii;Vriesea incurvata 80–1100 Izecksohn 1993,Peixoto1995, Fusinatto et al. 2008,Per.Obs.
Dendrophryniscus
brevipollicatus
LC Neoregelia sp. < 900 Izecksohn 1993,Peixoto1995, Fusinatto et al. 2008,Per.Obs.
Dendrophryniscus carvalhoi EN Vriesea simplex 800–1135 Izecksohn 1993,Peixoto1995, 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,Peixoto1995
Frostius erythrophthalmus* DD Unidentified 140–920 Pimenta and Caramaschi 2007
Frostius pernambucensis LC Vriesea noblickii; Nidularium sp. < 800 Cruz and Peixoto 1982,Peixoto1995, Juncá and Borges 2002,Juncá2006
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
(= Wittrockia smithii); N. procerum
655–850 Bornschein et al. 2015
Melanophryniscus
xanthostomus
DD** Aechmea distichantha;A. gamosepala;Vriesea incurvata;
V. Philippocoburgi
565–1275 Bornschein et al. 2015
Cycloramphidae
Crossodactylodes bokermanni NT Vriesea morreni 800–1477 Peixoto 1982,Frost2016,Per.Obs.
Crossodactylodes itambe DD Vri es ea me du s a 1836–2062 Barata et al. 2013, Santos et al. 2017
Crossodactylodes izecksohni NT Aechmea capixabae; Aechmea lamarchei; Edmundoa
lindenii; Neoregelia guttata; N. macrosepala;
N. pauciflora; Nidularium cariacicaensis;
Vriesea aff. atra; V. bituminosa; V. ensiformis; V. gracilior;
V. vagans
650–933 Peixoto 1982,Peixoto1995,Pertelet al.2006,Per.Obs.
Crossodactylodes pintoi DD Unidentified 1200 Peixoto 1982,Peixoto1995
Crossodactylodes
septentrionalis
NE Unidentified > 930 Teixeira et al. 2013
Dendrobatidae
Ameerega andina DD Unidentified 1700–2020 Myers and Burrowes 1987,Frost2016
Andinobates daleswansoni VU Unidentified 1800–2000 Rueda-Almonacid et al. 2006, Brown et al. 2011
Andinobates dorisswansoni* CR Unidentified 1780 Rueda-Almonacid et al. 2006, Brown et al. 2011
Andinobates minutus LC Unidentified < 1000 Summers and McKeon 2004,Brownetal.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
Host bromeliads and their associated frog species: Further considerations on the importance of species interactions... 203

Tab l e 1 (continued)
Frogs IUCN
category
Bromeliad host Altitudinal
distribution
(m a.s.l.)
Source
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 Vr ies ea sp., Hohenbergia sp., Guzmania sp. 650–850 Drewry and Jones 1976,Joglar1998
Eleutherodactylus
guantanamera
VU Tillandsia sp. 60–1150 Hedges et al. 1992
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
lindenii
500–1800 Duellman and Maness 1980,Pertelet al.2006, Heyer et al. 1990,Frost2016,Per.
Obs.
Fritziana aff. fissilis Vriesea platynema 448–850 Franz and Mello 2015
Fritziana goeldii LC Alcantarea imperialis; Aechmaea nudicaulis;
Aechmea lamarchei; Vriesea aff. a tra
430–1220 Lutz 1954, Duellman and Maness 1980,Peixoto1995,Frost2016,Per.Obs.
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,Frost2016
Gastrotheca ochoai DD Unidentified 2745–3080 Duellman 1979, Ângulo et al. 2004,Frost2016
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,Frost2016
Bromeliohyla dendroscarta CR Unidentified 450–1900 Duellman 1970, Altig and McDiarmid 1999,Frost2016
Dendropsophus bromeliaceus DD** Aechmea capixabae;Aechmea lamarchei;Aechmea pineliana;
Alcantarea extensa;Neoregelia pauciflora;Racinaeae
spiculosa;Vriesea bituminosa;Vriesea morrenii;
Vriesea ruschii;Vrie se a aff. Atra;Vriesea ensiformis;
Vriesea vagans;Nidularium cariacicaense;Nidularium
espiritosantensis;Nidularium sp.
745–922 Ferreira et al. 2015
Isthmohyla melacaena NT Unidentified 1370–1990 McCranie and Castaneda 2006,Frost2016
Isthmohyla picadoi NT Unidentified 1900–2650 Dunn 1937, Duellman 1970,Lips1998, Savage 2002, Stuckert et al. 2009,Frost2016
Isthmohyla zetecki NT Unidentified 1200–1804 Dunn 1937, Duellman 1970, Savage 2002,Frost2016
Osteocephalus deridens LC Aechmea zebrina; A. chantinii 250–600 Jungfer et al. 2000, Lehtinen et al. 2004,Frost2016
Osteocephalus fuscifacies DD Aechmea zebrina 250–600 Jungfer et al. 2000, McCracken and Forstner 2014,Frost2016
Tepuihyla exophthalma DD Brocchinia sp. 585–1550 Smith and Noonan 2001, MacCulloch and Lathrop 2005,Frost2016
Osteocephalus planiceps LC Aechmea zebrina 200–700 Guayasamin et al. 2006, McCracken and Forstner 2006,2008,2014,Frost2016
Osteopilus crucialis EN Hohenbergia urbiana 0–1200 Garrick et al. 1985,Hedges1987,Frost2016
Osteopilus marianae EN Tillandsia sp. 120–880 Hedges 1987,Frost2016
Osteopilus ocellatus LC Tillandsia deppeana; Hohenbergia fawcettii 0–1500 Laessle 1961,Lannooetal.1987,Frost2016
Osteopilus wilderi EN Tailândia sp. 120–880 Laessle 1961,Hedges1987,Crombie1999,Frost2016
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,Frost2016
Phyllodytes edelmoi NT Portea leptantha 0 Peixoto et al. 2003,Frost2016, Ruano-Farjado et al. 2016
Phyllodytes gyrinaethes CR Unidentified 0–650 Peixoto et al. 2003,Frost2016
Phyllodytes kautskyi LC Aechmea nudicaulis; A. blanchetiana; A. phanerophlebia;
A. chlorophyla
22–650 Peixoto and Cruz 1988, Simon and Gasparini 2003,Simonand
Peres 2012
Phyllodytes luteolus LC Aechmea blanchetiana; A. nudicaulis; A. saxicola;
A. victoriana; Vrisea procera;
V. neoglutinosa; Alcantaraea extensa; Hohenbergia
augusta; Quesnelia quesneliana
0–650 Teixeira et al. 1997,Eterovick1999,PappandPapp2000,Schineiderand
Tei xe ira 2001,
Juncá and Borges 2002,F
rost2016
204 Sabagh L.T. et al.

Tab l e 1 (continued)
Frogs IUCN
category
Bromeliad host Altitudinal
distribution
(m a.s.l.)
Source
Phyllodytes melanomystax LC Hohenbergia littoralis; Aechmea aquilega 0–10 Caramaschi et al. 1992,Juncá2006,Frost2016, Cunha and Napoli 2016
Phyllodytes punctatus DD Hohenbergia sp. 0–10 Caramaschi and Peixoto 2004,Caldasetal.2011,Frost2016
Phyllodytes tuberculosus DD Unidentified 997 Caramaschi and Peixoto 2004, Caramaschi et al. 2004,Frost2016
Phyllodytes wuchereri DD Unidentified 0–815 Caramaschi et al. 2004, Magalhães et al. 2015,Frost2016
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,Peixoto1995
Ololygon arduoa DD Alcantarea sp.; Vriesea ruschii; Vriesea bituminosa; V. morrenii;
V. vagans; V. aff. a tra; Quesnelia quesneliana
654–921 Pertel et al. 2010, Lacerda et al. 2015
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.;
Neoregelia cruenta; Alcantarea glauziouiana
0–220 Peixoto 1987, Silva et al. 1988, Oliveira and Navas 2004,Teixeiraetal.2006,
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;
Edmundoa lindenii; Neoregelia concentrica; Vrisea inflata;
V. philippocoburgii.
450–1220 Peixoto 1987,Per.Obs.
Microhylidae
Ctenophryne carpish EN Unidentified 2750–2960 Lehr and Trueb 2007,Lehretal.2007,Frost2016
Chiasmocleis antenori LC Guzmania weberbaueri 800–1500 Krügel and Richter 1995,Frost2016
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... 205

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

probability of extinction (see Koh et al. 2004). Given this, the
identification of the bromeliad species that host bromeligenous
frogs should be a priority for the conservation of these mutual-
istic species. We recommend that concerted research efforts
should include both studies on the identification of the host
species and also investigations of frog selectivity to determine
the threshold of vulnerability of the different frog species.
In mutualistic networks, the understanding of species inter-
actions is important for determining the likelihood of extinc-
tion cascades. We propose that the conservation of
bromeligenous frogs and their bromeliad hosts should focus
on the development of integrated strategies for the protection
of mutualisms. Specifically, three principal measures are need-
ed: (1) the identification of the bromeliad species used by
frogs, and the degree of mutualism; (2) the assessment of the
conservation status of bromeliads that host frogs, and (3) the
publication of records by scientific journals that provide infor-
mation on the presence of bromeligenous frogs and their tad-
poles in bromeliad host species, and the identification of the
bromeliad hosts to species level along with descriptions of any
new bromeligenous frogs. In addition researchers should de-
posit a voucher bromeliad specimen that is host to a known
frog in a recognized herbarium. We recommend that these
vouchers should be cited in any research papers and photo-
graphs of the bromeliads in vivo could also be added to de-
scriptive papers, if necessary as supplementary material.
In conclusion, our findings emphasise the importance of
the documentation of the interactions between bromeligenous
frogs and their respective bromeliad hosts to guarantee the
conservation of these mutualistic relationships and avoid co-
extinctions. Bromeliads usually host many other endemic
groups of animals (Lopez et al. 2009), and the conservation
of all these associated organisms may be the only way to
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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