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Poison frogs traded and maintained by U.S. private breeders

Authors:
  • Illinois Natural History Survey
Herpetological Review 52(4), 2021
HERPETOCULTURE 779
Acknowledgments.––Support for this study came from the Ontario
Ministy of Natural Resources and Forestry (OMNRF) and Environment
Canada. We thank Bruce Pauli from Environment and Climate
Change Canada for his thoughtful advice on tadpole rearing. We
thank J. Benbahtane, N. Jreidini, A. Zerafa, V. Tawa, E. Forget-Klein, D.
Shaban, T. Pulciano, A. Botsko, M. Martini, K. Kwaku, A. Brimacombe,
C. Berruezo i Llacuna, S. Thivierge, J. Purdy, A. Malet, L. Meehan, J.
Cuffaro, E. Jaeger, P. Harindranath, G. Rimok and R. Tremblay for their
assistance in tadpole rearing and mesocosm maintance, as well as
Ontario Parks, OMNRF and the staff at Long Point Provincial Park for
logistical support. This research was carried out in accordance with
McGill University Animal Use Protocol 4569 and permits from OMNRF
and Environment Canada. We also acknowledge the traditional owners
of the land on which we work; Long Point Provincial Park is situated
on the traditional territories of the Mississauga and Haudenosaunee
nations, and McGill University is located on the traditional territories
of the Haudenosaunee and Anishinabeg nations.
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© 2021 by Society for the Study of Amphibians and Reptiles
Poison Frogs Traded and Maintained by U.S. Private Breeders
Wildlife trade and the collection of wild animals for pets are
contributing to the global loss of biodiversity (Bush et al. 2014;
Scheffers et al. 2019; Morton et al. 2021). Most studies on the
impacts of the pet trade focus on birds, reptiles, and fish, but
there is also a sizeable market for amphibians (Carpenter et al.
2014). Amphibian trade has been linked to overexploitation of
wild populations, invasive species introductions, and the spread
of infectious diseases (Rowley et al. 2016; Wombwell et al. 2016;
Lockwood et al. 2019), but there could also be conservation
benefits. For example, consumer demand for threatened species
can generate funds for their conservation through biocommerce
programs (Yeager et al. 2020) and harvesting wild amphibians
for the pet trade could contribute to sustainable local livelihood
strategies in biodiverse developing countries (Robinson et al.
2018). Considering amphibians are one of the most threatened
vertebrate groups, with nearly 20% of all species on the brink of
extinction (Ceballos et al. 2020), understanding trade dynamics
of widely kept species is necessary for identifying threats and
informing policy, especially when weighing the costs and benefits
of the pet trade to both people and the environment.
Of all amphibians, poison frogs (superfamily Dendrobatoidea)
are some of the most popular to keep in captivity because of
their attractive aposematic coloration and diurnal behavior
(Mohanty and Measey 2019). Aquarium enthusiasts in Germany
and the Netherlands pioneered the poison frog hobby during
the early 1970s (e.g., Polder 1973; Broodman 1974; Zimmermann
1974), with the first frogs commercially available alongside
exports of tropical fish from South America. English language
literature describing poison frog captive care began appearing
in the mid-1980s with the rise of the pet reptile industry (e.g.,
Ensman 1985; Zimmermann 1986). In 1987, growing demand
and concern that overcollection could deplete wild populations
led the family Dendrobatidae to be added to the Convention on
International Trade in Endangered Species of Wild Fauna and
Flora (CITES; Gorzula 1996), though barely 100 people in the
U.S. were recorded keeping poison frogs at that time (Bertram
1988). Today, an estimated 50,000–100,000 people in the U.S. keep
poison frogs (Z. Brinks, pers. comm), with large numbers bred
domestically to meet demand. At the same time, private collectors
in the U.S. and Europe widely acknowledge the founding stock
of many commonly kept poison frogs originated through illicit
DEVIN EDMONDS
Illinois Natural History Survey, Prairie Research Institute, Champaign,
Illinois 61820, USA; University of Illinois at Urbana-Champaign,
Department of Natural Resources and Environmental Sciences,
Champaign, Illinois 61820, USA; e-mail: dae2@illinois.edu
Herpetological Review 52(4), 2021
780 HERPETOCULTURE
means (Pepper et al. 2007). By some estimates the illegal trade
makes up 10% of poison frog trade volume in Europe (Auliya
et al. 2016). In the case of the Critically Endangered Lehmann’s
Poison Frog (Oophaga lehmanni), overexploitation has been
linked to reduced genetic diversity in wild populations, with ca.
81,000 individuals extracted over the last four decades, leading to
population declines and extirpation of the population at the type
locality (Betancourth-Cundar et al. 2020).
Increasing awareness about the negative impacts of
harvesting wildlife for the pet trade has led to a growing push
to supply consumers with animals from sustainable sources
(Pasmans et al. 2017; Yeager et al. 2020). Poison frog breeding
ventures have been developed in Colombia, Ecuador, and Peru,
which aim to curb illegal trade and, in some cases, fund habitat
protection with their profits (Tapley et al. 2011; Sinovas and Price
2015). However, illicit trade could undermine such sustainable
breeding operations. Indeed, the criteria needed for wildlife
farming to have conservation benefits often are not met owing
to ongoing illegal trade and wildlife poaching (Tensen 2016).
Ranching and breeding programs supplying the international pet
trade also sometimes are used to launder wild-caught animals as
captive-bred (Bulte and Damania 2005; Lyons and Natusch 2011;
Robinson et al. 2015). Additionally, high-value species of poison
frog have been documented entering the trade illegally ahead
of legal imports (Pepper et al. 2007), filling consumer demand
with smuggled frogs and jeopardizing the viability of breeding
operations in range countries. Considered altogether, the negative
effects of the trade could outweigh possible conservation benefits
depending on the scale and scope of illicit activity.
Despite the size of the poison-frog hobby today, there are few
records of the frogs maintained in private collections and their
origins. Discrepancies in CITES records related to the illegal
trade obscure frog sources further, with wild animals laundered
through Europe or Asia and then imported to the U.S. as captive-
bred (Nijman and Shepherd 2010). Furthermore, some species
are polymorphic, with private collectors managing breeding
groups to represent distinct naturally occurring geographic color
morphs. In some cases, color variants appearing in U.S. collec-
tions are known to occur only in countries that have not allowed
their export. Thus, species exported from a native country but
with a phenotype matching those known from a different country
make it challenging to identify the true level of illicit activity when
wildlife trade is monitored mainly at the species or genus level.
The purpose of this article is to document the poison frogs main-
tained and bred in U.S. collections, determine the ways they ini-
tially entered the trade, and examine how the origins and sources
of new poison frogs have changed over the last thirty years.
materiaLs and metHOds
The data used to summarize poison frog trade included:
1) primary sources such as social media group posts, internet
forums, printed literature, and unstructured interviews with
private breeders/dealers, 2) the CITES trade database, 3) the
IUCN Red List, and 4) the U.S. Fish and Wildlife Service (USFWS)
Law Enforcement Management Information System (LEMIS). To
compile a list of the different poison frogs in captivity, I relied first
on personal knowledge and recorded familiar species and color
morphs. I then added to the list by searching internet forums and
social media groups, noting the species and color morphs traded
as well as when they first began appearing online. The Way Back
Machine (Internet Archive 2021) was used to document poison
taBLe 1. All poison frogs (superfamily Dendrobatoidea) maintained
and bred by U.S. private breeders during 1990–2020 and their
current IUCN Red List category. “Morphs” is the number of discrete
captive populations collectors were intentionally breeding separate
from others, usually corresponding to a wild phenotype and/or a
particular import from a known source. “Currently kept?” indicates
if there was evidence a species was in a U.S. collection in 2015–2020.
Taxon Morphs Red List category Currently kept?
Adelphobates castaneoticus 1 Least Concern Yes
Adelphobates galactonotus 10 Least Concern Yes
Adelphobates quinquevittatus 1 Least Concern Yes
Allobates femoralis 2 Least Concern Yes
Allobates zaparo 2 Least Concern Yes
Ameerega altamazonica 2 N/A Yes
Ameerega bassleri 5 Vulnerable Yes
Ameerega bilinguis 2 Least Concern Yes
Ameerega cainarachi 1 Endangered Yes
Ameerega hahneli 2 Least Concern Yes
Ameerega pepperi 4 Vulnerable Yes
Ameerega picta 1 Least Concern No
Ameerega pongoensis 1 Vulnerable Yes
Ameerega silverstonei 2 Endangered Yes
Ameerega trivittata 5 Least Concern Yes
Andinobates bombetes 1 Vulnerable No
Andinobates fulguritus 1 Least Concern No
Andinobates minutus 1 Least Concern No
Dendrobates auratus 33 Least Concern Yes
Dendrobates leucomelas 6 Least Concern Yes
Dendrobates tinctorius 42 Least Concern Yes
Dendrobates truncatus 3 Least Concern Yes
Epipedobates anthonyi 12 Near Threatened Yes
Epipedobates boulengeri 2 Least Concern Yes
Epipedobates darwinwallacei 2 N/A Yes
Epipedobates tricolor 5 Vulnerable Yes
Excidobates mysteriosus 1 Endangered Yes
Hyloxalus azureiventris 2 Endangered Yes
Oophaga arborea 1 Critically Endangered Maybe
Oophaga granulifera 7 Vulnerable Yes
Oophaga histrionica 23 Critically Endangered Yes
Oophaga lehmanni 6 Critically Endangered Yes
Oophaga pumilio 85 Least Concern Yes
Oophaga speciosa 1 Extinct No
Oophaga sylvatica 15 Near Threatened Yes
Oophaga vicentei 2 Endangered Yes
Phyllobates aurotaenia 5 Least Concern Yes
Phyllobates bicolor 5 Endangered Yes
Phyllobates lugubris 2 Least Concern Yes
Phyllobates terribilis 5 Endangered Yes
Phyllobates vittatus 2 Vulnerable Yes
Ranitomeya amazonica 7 Data Deficient Yes
Ranitomeya benedicta 3 Vulnerable Yes
Ranitomeya fantastica 10 Vulnerable Yes
Ranitomeya flavovittata 2 Least Concern Yes
Ranitomeya imitator 15 Least Concern Yes
Ranitomeya reticulata 6 Least Concern Yes
Ranitomeya sirensis 8 Least Concern Yes
Ranitomeya summersi 2 Endangered Yes
Ranitomeya uakarii 3 Least Concern Yes
Ranitomeya vanzolinii 2 Least Concern Yes
Ranitomeya variabilis 8 Data Deficient Yes
Ranitomeya ventrimaculata 1 Least Concern Yes
Herpetological Review 52(4), 2021
HERPETOCULTURE 781
frogs kept on now-defunct websites dating back to 1998, with a
focus on U.S. trade because of its accessibility and presence as
one of the largest markets for pet amphibians (Schlaepfer et al.
2005; Herrel and Van Der Meijden 2014). To examine the types
of frogs kept prior to widespread internet use, I reviewed animal
dealer price lists, pet trade books and magazines (e.g., Tropical
Fish Hobbyist, Reptiles), the American Dendrobatid Group
newsletter (running 1992–2000; available at: archive.org/details/
americandendrobatidgroup), and the International Society
for the Study of Dendrobatids newsletter (running 1988–1992;
available at: archive.org/details/issd_bulletin). For each species,
I recorded the trade names of color morphs, information about
their origin in the U.S. (how they were imported, year of import,
etc.), and when the color morph was most recently maintained
in collections. A color morph was defined as a distinct captive
population that collectors were intentionally breeding separate
from others, regardless of appearance. Synonyms of trade
names were noted and combined, and I updated the taxonomy
of old records to agree with Frost (2021). I then circulated the
spreadsheet and made inquiries to 29 current or former private
breeders and/or dealers in the U.S., as well as one breeder in
Canada and one in the Netherlands. Specific color morphs were
considered currently in U.S. collections if there was evidence
(e.g., a social media post, classifieds ad, confirmation from a
private breeder, etc.) they had been kept during 2015–2020.
After compiling the dataset from primary sources, I compared
the time of arrival to records of U.S. imports in the CITES Trade
Database (CITES 2020). Recommendations by Robinson and Sino-
vas (2018) were followed about interpreting CITES data. In some
cases, it was not possible to confirm the year when a color morph
was first imported because CITES only records data to the species-
or genus-level and has no way of recording successfully smuggled
animals. However, by working with the network of private breed-
ers, I was able to infer the year of first arrival in the U.S. to a five-
year range or less for all color morphs and species. The earliest
year in the five-year range was used to summarize how trade has
changed through time. For example, if a frog first became estab-
lished at some point during 1992–1996, the year 1992 was used
as the year of arrival for analyses. Additionally, many species and
color morphs were imported or entered U.S. collections through
a variety of different pathways. For example, new color morphs
of a species were sometimes smuggled to the U.S. years before
legal commercial imports arrived, with frogs from both sources
subsequently bred together. Therefore, for color morphs that ar-
rived from multiple sources and had since been bred together, I
grouped their origin into a single source corresponding to the ear-
liest way they arrived and became established.
To examine whether threatened species were more likely
to be kept in private collections, I compared the IUCN Red List
(2020) status of traded dendrobatids with the IUCN Red List
status of non-traded species. I excluded Ameerega altamazonica
and Epipedobates darwinwallacei from the comparison because
the two species are not recorded in the IUCN Red List. Allobates
femoralis and A. zaparo were also excluded because they are in the
poison frog family Aromobatidae rather than Dendrobatidae.
Lastly, the LEMIS database was used to examine U.S. import
volume. For the years 2000–2014, I accessed the LEMIS database
made available by the EcoHealth Alliance (see Smith et al. 2017)
and combined those data with data from the years 2015–2019
received from a Freedom of Information Act request with USFWS.
Data from LEMIS for 2020 were unavailable at the time of the
request. Data was compiled and summarized using Google Sheets,
Microsoft Excel, and R version 3.6.2 (R Core Team 2019).
resuLts
From 1990–2020, 378 color morphs of 53 poison frog species
were maintained in U.S. private collections (Table 1). The spe-
cies maintained in collections increased 108% (23 pre-1990; 48
in 2020), and the number of different color morphs by 766% (41
pre-1990; 355 in 2020). Five species and 23 color morphs were
in U.S. collections but are no longer kept, including one recent-
ly extinct species (Oophaga speciosa; IUCN 2020). For 47 color
morphs of 19 species, I was unable to confirm if they currently are
Fig. 1. The IUCN Red List status of 49 poison frog species in the fam-
ily Dendrobatidae that were traded 1990–2020 (right) compared to
the IUCN Red List status for the remaining 142 non-traded species
(left). Four traded species (Allobates femoralis, A. zaparo, Ameerega
altamazonica, and Epipedobates darwinwallacei) were excluded
from the comparison because they are not recorded in Dendrobati-
dae by the IUCN Red List.
Fig. 2. The origin of all color morphs of poison frogs (Dendrobatoi-
dea) maintained in U.S. private collections 1990–2020. The sources
correspond to the four categories A–D in Table 2.
Herpetological Review 52(4), 2021
782 HERPETOCULTURE
in collections. Four species made up more than half of all types
of poison frogs kept: Oophaga pumilio (85 morphs), Dendrobates
tinctorius (42 morphs), D. auratus (33 morphs), and O. histrionica
(23 morphs). The full dataset of traded poison frog species, color
morphs, and notes justifying origins in collections is available at:
doi.org/10.13012/B2IDB-4717502_V1.
The proportion of threatened species (Critically Endangered,
Endangered, and Vulnerable Red List categories) was similar
between traded and non-traded species (Fig. 1). The IUCN Red
List assessed 39% of traded species as threatened versus 38% of
non-traded species. However, non-traded species were composed
of a greater proportion of Data Deficient species; 4% of traded
species were Data Deficient compared to 37% of non-traded
species (Fig. 1).
Poison frogs have entered U.S. amphibian collections ten dif-
ferent ways (Table 2). New types of frogs originating from both
legal wild commercial collection and smuggling decreased after
2000, coinciding with the development of breeding and ranching
operations (Figs. 2, 3). There were 37 species represented by 109
color morphs that originated from breeding and ranching pro-
grams in native range countries. The first frogs from such breeding
programs were imported to the U.S. in 2006. An additional 24 new
color morphs originated after 1990 solely as wild frogs exported
for commercial purposes, most of which (20 of 24) were color
morphs of Dendrobates tinctorius. Six color morphs of four spe-
cies were imported from Europe but appeared to have been off-
spring from legal wild commercial collection. Two color morphs
of D. auratus originated in private collections after being released
from a zoological institution to private breeders in the early 1990s.
For 24 color morphs of 11 species entering collections post-1990,
there were multiple origins and private breeders did not or no lon-
ger distinguished between frogs from the various sources.
Six illicit pathways were used to source poison frogs for U.S.
collectors (Table 2). The two most common illicit trades routes
were wild-caught frogs misleadingly imported as bred in captiv-
ity or ranched from native range countries (85 color morphs of 8
species), and smuggled frogs or their descendants imported from
Europe (74 morphs of 31 species). I also traced the first availability
of 22 color morphs for 8 species to instances of direct smuggling to
the U.S., all but one of which occurred before 2005. Of the 96 color
morphs originating from smuggling, more than half were native
to three countries: Peru (23 morphs), Panama (17 morphs), and
Ecuador (14 morphs; Fig. 4).
Data from the U.S. Fish and Wildlife Service showed that
142,211 individual poison frogs were imported during 2000–2019
(Figs. 5, 6). Annual import quantity peaked in 2006–2008, driven
by two species: D. auratus and O. pumilio. Together, imports of
D. auratus and O. pumilio from a single exporter in Panama ac-
counted for more than half (85,348 individuals) of all poison
frogs imported to the U.S. during 2000–2019. Of the Panamanian
frogs, 94.5% of D. auratus and 98.6% of O. pumilio were recorded
as captive-bred; however, private breeders widely believed most
were wild-caught due to the age, condition, and quantity of frogs
arriving.
disCussiOn
The poison frogs traded among U.S. collectors originated from
diverse sources. Species and color morphs new to the trade that
were descended from smuggled animals decreased over the last
three decades, coinciding with businesses in Colombia, Ecuador,
taBLe 2. Ten pathways poison frogs enter U.S. private collections, categorized by the potential benefit or detriment to natural resource management
and conservation.
Category Pathway
A. Responsible trade with an intended conservation benefit 1. Imported or descended from an established breeding or ranching
program in the native range of the species that funds conservation
efforts.
B. Responsible trade in agreement with regulations and quota systems 2. Imported as wild-caught frogs for commercial purposes from a
country in the species native range and in agreement with
trade regulations.
3. Imported from a European country but descended from animals
most likely originally collected in a legal manner (e.g., regulated
commercial harvest as above).
4. Collected for a zoological institution or university and intentionally
distributed to private breeders.
C. Illicit trade detrimental to good governance and responsible natural 5. Misidentified wild-caught frogs imported for commercial purposes
resource management from a native range country.
6. Imported from a country in the native range of the species but for
which the color morph is only known to occur outside the exporting
country.
7. Imported from a breeding or ranching program in the native range
of the species, yet the quantity, condition, and age of animals imported
suggested they were likely collected from wild populations.
8. Collected for a zoological institution or university and distributed to
the trade in violation with agreements from the country of origin or the
institution.
D. Illicit trade as above but also involving explicit wildlife poaching 9. Imported from Europe or Asia but descended from smuggled
animals, or smuggled animals themselves, including those confiscated
by, surrendered to, or gifted from a zoological institution and released
to European private breeders (i.e., laundered frogs).
10. Wild frogs smuggled directly to the U.S.
Herpetological Review 52(4), 2021
HERPETOCULTURE 783
and Peru developing captive breeding and ranching programs (Si-
novas et al. 2017; Steffens 2018; Yeager et al. 2020). While breeding
programs in native range countries increased, species and color
morphs new to the trade that originated from legal wild-caught
imports decreased. Such trends mirror patterns in the global trade
of live reptiles; between 2001 and 2012 there was a 70% decrease
in wild-caught reptiles and 50-fold increase in ranched reptiles
(Robinson et al. 2015). The trend in new poison frogs entering
collections from responsible sources is encouraging, but illegal
collection also continues (Fig. 2). In some cases, smugglers have
targeted recently described species and color morphs in the sci-
entific literature (Auliya et al. 2016). Smuggling has not only im-
pacted newly discovered populations but also damaged habitat,
with trees selectively cutdown to access the phytotelmata of bro-
meliads where high value poison frogs are most easily captured
(Brown et al. 2011). Peru was the native range country for the
greatest number of poison frogs in U.S. collections descending
from smuggled animals, followed by Panama and Ecuador.
Regarding trade volume, most poison frogs in U.S. collections
are almost certainly bred domestically (Carpenter et al. 2014).
Still, a Panama business accounted for the largest quantity of
poison frog imports since 2000. Private breeders widely believed
the Panama exporter was laundering wild-caught D. auratus
and O. pumilio as captive-bred, which is a common method
for illegally exploiting wildlife populations (Lyons and Natusch
2011; Janssen and Chng 2018). As evident by the large volume
of frogs imported, there is likely sufficient demand to develop
legitimate captive breeding or ranching programs in Panama
with a conservation benefit, similar to ventures in Colombia,
Ecuador, and Peru. Yet, without enforcement of trade regulations
or pressure from consumers, such a program is unlikely to
develop. Alternatively, considering D. auratus and O. pumilio
are assessed as Least Concern by the IUCN Red List (IUCN 2020)
and often are abundant in secondary or degraded habitat (Cove
and Spínola 2013; McKone et al. 2014), wild populations might
easily support regulated harvests. However, if authorities wrongly
believe exported frogs are captive-bred rather than wild-caught,
unsustainably high export quotas could put wild populations at
risk, especially color morphs or localities in great demand from
collectors. Indeed, overexploitation of wild populations for the
pet trade has caused declines in other amphibian species of
commercial value (e.g., Andreone et al. 2006; Rowley et al. 2016).
For people who keep poison frogs as a hobby, it is important to
avoid purchasing frogs from questionable sources, not only
because of the impact unregulated harvest could have on wild
populations, but also because the illicit trade puts legal trade at
risk of further regulation (Wyatt et al. 2018).
Emerging infectious diseases and invasive species also are
threats linked to the amphibian pet trade, but poison frogs likely
present less risk than other commonly kept species. Notably, the
global spread of the chytrid fungus Batrachochytrium dendroba-
tidis is associated with the amphibian trade (Fisher and Garner
2007; Schloegel et al. 2009; Wombwell et al. 2016), and the chytrid
fungus B. salamandrivorans in Europe emerged through the im-
portation of pet amphibians from Asia (Martel et al. 2014; Sabi-
no-Pinto et al. 2015). Still, compared to other traded species, the
quantity of poison frogs imported to the U.S. is relatively small.
For example, during 2001–2009 nearly 9 million Dwarf Water
Frogs (Hymenochirus curtipes) were imported to the U.S. (Herrel
Fig. 3. The origin of all color morphs of poison frogs (Dendrobatoidea)
maintained in U.S. private collections 1990–2020. The sources cor-
respond to the categories in Table 2: 1) captive breeding and ranch-
ing programs with an intended conservation benefit; 2) wild-caught
commercial imports; 3) non-smuggled European imports; 4) trans-
parent release from a zoo or research program; 5) misidentified wild-
caught commercial imports; 6) wild-caught commercial imports of a
color morph only known to occur outside the exporting country; 7)
wild-caught frogs imported from a native country as captive-bred or
ranched; 8) descended from a research program which was not sup-
posed to release frogs to the public; 9) European imports of smuggled
or laundered frogs; 10) frogs directly smuggled to the U.S.
Fig. 4. The number of new types (color morphs and species) of poi-
son frogs (Dendrobatoidea) descending from smuggled animals
which entered U.S. collections 1990–2020 by their native country.
The figure shows only frogs from sources 9 and 10 in Table 2, cor-
responding either to frogs that were directly smuggled to the U.S. or
were laundered first through a European or Asian country.
Herpetological Review 52(4), 2021
784 HERPETOCULTURE
and Van Der Meijden 2014). During the same period, imports for
the entire poison frog family Dendrobatidae numbered less than
80,000 individuals. Consequently, poison frogs likely warrant
less concern than other heavily imported species with regard to
spreading infectious diseases internationally. The amphibian pet
trade also is responsible for introducing invasive species (Kopecký
et al. 2016; Lockwood et al. 2019). Green and black poison frogs
(D. auratus) have been established in Hawaii after an unsuccess-
ful release for pest control in the early 20th century (Oliver and
Shaw 1953). Nevertheless, poison frogs have a small body size and
are relatively expensive, meaning they are less likely to be released
by pet owners than are other commonly kept amphibian species,
thus posing a lower risk of becoming established outside their na-
tive range through the pet trade (Stringham and Lockwood 2018).
Gorzula (1996) provided an overview of poison frogs traded
during the first seven years after addition to CITES (1987–1993),
concluding that the number of frogs traded “would not have filled
a large trash can” and therefore was unlikely to be impacting wild
populations. A similar outlook was common among the scientific
community in the 1980s (e.g., Picket 1987; Mrosovsky 1988),
with researchers only beginning to recognize that widespread
amphibian extinctions and declines were a rising global
phenomenon (Blaustein and Wake 1990; Wake 1991). Twenty-five
years later, we better understand the severity of what has been
dubbed the amphibian extinction crisis and have documented
ways the live amphibian trade can exacerbate the problem
(e.g., Fitzpatrick et al. 2018; Stringham and Lockwood 2018).
Concurrently, many times more people now keep poison frogs,
with demand for pet amphibians on the rise (Measey et al. 2019).
Considering responsible trade can have conservation benefits
and blanket trade bans do not usually work (Garner et al. 2009;
Pasmans et al. 2017), policies should aim to ensure amphibians in
the pet trade originate from sustainably-managed sources rather
than restrict trade overall. Further trade analyses are needed
to inform policy and should focus on the scale of domestic
production of pet amphibians, which is not captured in CITES
or LEMIS data (Schlaepfer et al. 2005), as well as on the potential
livelihood benefits to local people who catch and export wild
amphibians for the pet trade (Robinson et al. 2018). Nicaragua,
Panama, and Suriname supply the bulk of wild-caught poison
frogs to the trade and should be the focus of future field studies
examining trade impacts on wild populations.
Acknowledgments.–This project would not have been possible
without the time and trust of the private breeders and dealers who I
worked with to compile the dataset. Particularly, I would like to ac-
knowledge E. Malolepsy for lending me the International Society for
the Study of Dendrobatids newsletters to digitize and C. Powell for
providing digital copies of the American Dendrobatid Group newslet-
ter. Thank you to K. Garner and J. Mendelson for reviewing the manu-
script. The study protocol was reviewed by the Office for the Protection
of Research Subjects at the University of Illinois at Urbana-Champaign
and determined to not meet the criteria for Human Subjects Research.
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TESTUDINES — TURTLES
APALONE MUTICA (Smooth Softshell). FORAGING TRACES. Al-
though sit-and-wait strategies may sometimes be used, Apalone
are thought to primarily employ active foraging techniques as
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difficult to make due to their extreme shyness and wariness; how-
ever, observations of captive softshells can provide some insight
into their active foraging behavior.
I maintained several adult male and juvenile A. mutica over
several years in a 7 × 15 m outdoor enclosure located within the
species natural range in Searcy, Arkansas, USA. The enclosure
contained a ca. 5 m2 pool that varied in depth from 1–20 cm. The
softshells successively overwintered in the pool substrate and fed
and grew well on a diet of canned salmon and sardines. In addition,
the turtles foraged on various naturally occurring invertebrates in
the mixed sand and silt bottom substrate. The water was often
slightly cloudy due to the stirring of bottom sediments by foraging
activities of the softshells.
I occasionally observed a series of unusual whirl marks of
unknown origin in the pool substrate and in September 2014, I
discovered via a remote camera the source of the unusual marks.
I observed an adult male A. mutica actively foraging in the pool,
leaving behind the distinctive mosaic pattern of whirl marks in
its meandering path (Fig. 1). The whirl marks were created by
the turtle’s forelimbs as they were repeatedly extended forward
to a point directly anterior to the turtle’s snout and then drawn
back laterally in a breaststroke swimming motion, which drew
the claws shallowly through the substrate. The turtle appeared
to simultaneously probe the disturbed area with its snout and
periodically eat whatever may have been uncovered by the limb
movements. The turtle would then move forward a short distance
and repeat the peculiar foraging behavior. The forward movement
appeared to be made in a cohesive meandering path to thoroughly
search a small patch (outlined in Fig. 1) before moving on to a new
foraging patch.
I occasionally observed similar mosaic whirl traces in small
shallow, still-water pools on the lee end of sandbars on the
Kansas River near Lawrence, Kansas, but did not at the time
recognize what the peculiar patterns represented (MVP, unpubl.
data). Foraging traces likely may also be made in moving water,
the preferred habitat of A. mutica (Webb 1962, op. cit.; Ernst and
Lovich 2009, op. cit.), but probably are quickly obscured by the
moving water.
Why A. mutica sometimes confine their foraging in patches is
unknown. In the field, foraging A. mutica have been observed to
root in the substrate (Webb 1962, op. cit.; Plummer and Farrar 1981.
J. Herpetol. 15:175–179), but in no particular pattern. Confining
foraging to patches could possibly be related to the distribution of
prey in the substrate (Stephens and Krebs 1987. Foraging Theory.
HERPETOCULTURE NOTES
Fig. 1. A mosaic of whirling foraging traces (outlined) made by an
adult male Apalone mutica. Large arrow indicates foraging softshell;
small arrows indicate heads of three burrowed Apalone. Image taken
through cloudy water on 12 September 2014.
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