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Scientific classification Edit this classification
Domain: Eukaryota
Kingdom: Animalia
Phylum: Chordata
Class: Amphibia
Order: Anura
Family: Dendrobatidae
Genus: Oophaga
Species:
O. sylvatica
Binomial name
Oophaga sylvatica
(Funkhouser, 1956)[2]
Synonyms

Dendrobates histrionicus sylvaticus Funkhouser, 1956
Dendrobates sylvaticus Funkhouser, 1956

Oophaga sylvatica, sometimes known as its Spanish name diablito, is a species of frog in the family Dendrobatidae found in Southwestern Colombia and Northwestern Ecuador.[3] Its natural habitat is lowland and submontane rainforest; it can, however, survive in moderately degraded areas, at least in the more humid parts of its range. It is a very common frog in Colombia, but has disappeared from much of its Ecuadorian range. It is threatened by habitat loss (deforestation) and agricultural pollution. It is sometimes seen in the international pet trade.[4]

This species occurs in several color morphs. For example, the Bilsa Biological Station (operated by the Jatun Sacha Foundation) boasts three color morphs—red, yellow, and orange—within their 3000-ha protected area located within Ecuador's Mache and Chindul coastal mountain ranges.[citation needed]

Description

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Oophaga sylvatica only displays sexual dimorphism in body size, as both males and females typically having a snout-vent length of 26 - 38 mm, with the males being only slightly larger on average than females.[5][6] Amongst other closely-related species, they are the largest.[3] These species sport aposematic coloration, exhibiting both polytypic and polymorphic variation. Aposematic coloration serves as a visual warning to potential predators that the species is unpalatable. While the patterning of color varies widely, the colors themselves reliably exhibit chromatic and achromatic contrast. This wide range of pattern variation suggests roughly equal fitness for such variation. The range of colors that O. sylvatica displays is also considerably constrained to varying shades of orange, black, and other similar colors. Such coloration allows them to blend in with the mottled forest floor, where they are typically found. Their skin is smooth, with no webbing between any of their toes.[3]

Habitat and Distribution

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O. sylvatica is natively distributed in regions of Southwestern Colombia and Northwestern Ecuador. It inhabits humid tropical forests, mostly lowland and submontane rainforest.[3][4] These species are found up to 1000 meters above sea level.[5]

Conservation

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This species is able to tolerate living in some degraded regions such as plantations in the more humid parts of its habitat range.[3][4] Its habitat is threatened by deforestation for anthropogenic land use, including agriculture, logging, mining, human settlements, and pollution.[5] Last assessed by the IUCN, Oophaga sylvatica was categorized as a Near Threatened species, with its population trend decreasing.[4] There have been no significant conservation efforts as of date.

Population Structure, Speciation, and Phylogeny

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Oophaga sylvatica belongs to the family of Dendrobatidae, commonly called poison-dart frogs, characterized by their bright coloration and toxic alkaloids found in their skin. These frogs are diurnal creatures, demonstrate terrestrial egg laying, and exhibit behavioral parental care of eggs and tadpoles.[7] This family consists of 4 genera: Atopophrynus, Colostethus, Phyllobates, and Dendrobates.[8]

Also known as Dendrobates sylvaticus, the phylogenetic relationship for this species has been modified a couple of times, with most hypothetical models suggesting its closest relatives to be D. pumilio, D. arboreus, D. speciosus, and D. granuliferus.[9]

While sometimes considered to be a complex species due to its high levels of morphological variation, genetic studies suggest different populations of Oophaga sylvatica are in fact a single species. In populations studied in northwestern Ecuador, O. sylvatica was found to follow two main genetic lineages, separated by the Santiago River into northern and southern groups. The northern groups consist of San Antonio, Lita, Alto Tambo, Durango, and Otokiki. Genetic analyses revealed relatively high mitochondrial diversity but overall weak genetic differences. These populations were distributed fairly close to each other and those with overlapping regions often displayed a mix of the two population phenotypes. The southern populations consist of Felfa, Cristóbal Colón, Simón Bolívar, Quingüe, Cube, Puerto Quito, Santo Domingo, and La Maná. Genetic analyses revealed little mitochondrial diversity, suggesting the southern populations resulted from rapid radiation at some point in their history. Compared to the northern populations, the southern populations were found to be geographically distant. Both groups had significantly variable color diversity.[10]

Territoriality

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Male home ranges are typically restricted to small calling territories, found to be about 56% smaller than the home ranges of females. Males were found to also climb up to only 2 meters in height, whereas females could climb up to 10 meters in height. Despite this, when experimentally displaced from their territories, males demonstrated better homing accuracy on average, compared to females. This may be attributed to the androgen spillover hypothesis, which dictates that higher levels of androgen are correlated with better spatial abilities, as males were found to have higher levels of androgen on average.[11] Within their calling territories, males exhibit territorial and aggressive behaviors against other males of their own species.[7] Similar to other frogs, O. sylvatica is not a very migration-oriented species.[10]

Diet

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Oophaga sylvatica’s diet consists mainly of leaf litter arthropods. Researchers found in an Ecuadorian sample of this species that the majority of its diet consists of ants, ranging between 40% and 86%. A total of 44 ant genera were found, from 9 subfamilies, with the Myrmicinae subfamily constituting a majority.[12] Other insects the frog consumes include mites, springtails, and insect larvae.[13] The ant and mite species O. sylvatica consumes contributes to its accumulation of and variation in alkaloid toxins stored in its skin.[14]

Reproduction and Life Cycle

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Oophaga sylvatica males fertilize eggs externally.[5] As their eggs are laid in or near shallow pools on land, this species lays fewer and larger eggs than its water-laying counterparts, which is hypothesized to provide each egg with more resources to mature so that at the time of hatching, it has a greater chance of surviving on land, because tadpoles need water to survive.[7] Clutch sizes typically range between 30 to 46 eggs.[5] It typically has a lifespan of 2-8 years.[15]

Mating

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Within its territory, males produce mating calls between 6 AM and 7 PM.[3] Their calls are short in duration and high in frequency, averaging about 5 calls every second.[16] One study found call note durations about 90 ms, with frequencies ranging from 800 to 3000 Hz. The most common frequencies occurred from 1750 to 1950 Hz, and 2300 to 2450 Hz.[17] Males usually call from elevated perches.[16] A study published in 2014 suggests that because of the brightly-colored aposematism frogs like O. sylvatica present, they use this protection from predators to their advantage by evolving more diverse and complex mating calls.[18]

Once a female is attracted to a male’s territory, they engage in a series of mating behaviors, including pursuing and circling each other, crouching, and touching. During this ritual, the male leads the female to a suitable location for laying her eggs.[16] At the end of the mating ritual, copulation occurs without amplexus; instead, the male first deposits his sperm on the ground, for the female to lay her eggs on after.[5][19]

Parental Care

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Once the eggs are fertilized, the males are largely responsible for the caretaking of the eggs. He typically visits the clutch several times each day and secretes fluids onto the eggs to prevent desiccations, as they are laid on land. Closer to the time of hatching, females will visit the clutch more frequently. It is essential for the parent to be present when the eggs hatch, so the tadpoles can be transported to water, without which they cannot survive. Once the eggs hatch, tadpole transport and care becomes solely the female’s responsibility, without interaction or cooperation from the father. As suggested by their name, Oophaga, which translates to “egg” and “eat”, tadpoles only consume the trophic eggs produced by their mother until they are old enough to metamorphosize.[7]

Enemies

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While the predation of Oophaga sylvatica has not yet been explicitly studied, it is likely that they share possible predation threats with their close relatives such as Oophaga pumilio, which includes birds, reptiles, and arthropods with high-functioning visual abilities.[20][21]

There has been evidence of O. sylvatica infected by chytridiomycosis, a disease caused by the fungus chytrid that infects amphibians around the world.[4][22]

Toxins

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Oophaga sylvatica feed on insects such as ants and mites that contain lipophilic alkaloid toxins, and these toxins are then absorbed by the frog and used as a defense mechanism.[4] These frogs cannot produce the toxins by themselves. Proteomic profiling has revealed that the livers of these frogs produce high levels of specialized proteins like saxiphilin that may be involved in alkaloid sequestration.[4] Ingesting lipophilic alkaloids causes a dramatic increase in saxiphilin expression in the skin and liver of the frog.[5] Saxiphilin protein is likely involved in helping to transport the alkaloids from the digestive tract to the skin, where they are used in defense.[5] Oophaga sylvatica can sequester alkaloids in just 4 days compared to weeks in some other dendrobatid species such as the golden poison frog.[5] The alkaloids also cause them to give off vibrant colors.[23]

Deforestation can cause dietary changes in frog populations that live in deforested pastureland compared to frogs that live in the rainforest.[24] The diet of pastureland frogs has a much smaller variety of alkaloids in it due to a reduced variety of ants, mites, and termites available to feed on compared to rainforest frogs.[25] This translates to a reduced variety of alkaloids being sequestered in the pastureland frogs for their own defenses.[26]

This trait is shared amongst its phylogenetic family, as about 500 types of alkaloids have been identified from the skin extracts of various members of the Dendrobatidae family, representing over 20 distinct structural classes.[27] Amongst the toxins found in O. sylvatica are histrionicotoxins, indolizines, lehmizidines, and decahydroquinoline.[28] The toxins are found most abundantly in the frog’s skin granular glands, liver, muscles, and oocytes.[29] It has been suggested that the toxin’s presence in oocytes serve to provide offspring with toxic defense mechanisms early on, when they are growing and still depend on their mother’s trophic eggs for nourishment.[30]

There is ongoing research investigating how O. sylvatica is able to sequester and use alkaloid toxins, as well as how its consumption of such toxins alter its molecular physiology related to metabolic functions. After ingestion, the frog’s intestinal lining is designed to prevent passive absorption of toxins. Instead, they are transported through the blood via carrier proteins, and the lymph via chylomicrons, as these toxins are small and lipophilic. How exactly the toxins are able to arrive at the skin and be stored in granules is yet unknown, but researchers hypothesize this process likely involves coordination between various tissues and transport systems.[28][29]

While O. sylvatica harvests toxins from its diet for defensive use, its body must also strike a balance between usage and metabolism to prevent the organism itself from being poisoned. As such, proteomic profiling studies have found varying degrees of upregulation and downregulation of different metabolic-related proteins in these frogs, compared to non-toxic controls. Some drug-metabolizing proteins are found to be decreased, such as nicotinamide N-methyltransferase, found to detoxify xenobiotics, and cytochrome P450s, which are involved in small molecule metabolism. Meanwhile, others are increased, such as glutathione S-transferase kappa 1. There have also been a host of proteins found to be upregulated in expression that may play a role in alkaloid transport.[31] ApoA4 is an apolipoprotein that could also function as an alkaloid transporter. The complement system is also found to be more active, especially the C3 protein, which may enhance alkaloid absorption. Parallels have been drawn with CVF, the cobra venom factor that is activated by cobra venom. Heat shock proteins were found to be upregulated in the liver, which could be used to bind decahydroquinoline, a form of alkaloid toxin, or as a response to the destabilizing ability of alkaloids on other proteins.[28][29]

Alkaloids are commonly found to target voltage-gated sodium channels and nicotinamide acetylcholine receptors, and it has been commonly found that frog resistance to the toxins they use for defense is linked to mutations in such ion channels. Evidence shows downregulation of various ion channels in O. sylvatica, including the amiloride-sensitive sodium channel, the sodium-potassium pump, and TRPV2, which functions to detect noxious chemicals. The sodium-potassium channel in particular has been found to contain mutations in various animals exhibiting toxin resistance.[28][29]

References

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  1. ^ IUCN SSC Amphibian Specialist Group (2019). "Oophaga sylvatica". IUCN Red List of Threatened Species. 2019: e.T55203A85887077. doi:10.2305/IUCN.UK.2019-2.RLTS.T55203A85887077.en. Retrieved 17 November 2021.
  2. ^ "Oophaga sylvatica (Funkhouser, 1956)". Integrated Taxonomic Information System. Retrieved 2 September 2014.
  3. ^ a b c d e f Frost, Darrel R. (2014). "Oophaga sylvatica (Funkhouser, 1956)". Amphibian Species of the World: an Online Reference. Version 6.0. American Museum of Natural History. Retrieved 2 September 2014.
  4. ^ a b c d e f g IUCN (2016-08-02). "Oophaga sylvatica: IUCN SSC Amphibian Specialist Group: The IUCN Red List of Threatened Species 2019: e.T55203A85887077". doi:10.2305/iucn.uk.2019-2.rlts.t55203a85887077.en. {{cite journal}}: Cite journal requires |journal= (help) Cite error: The named reference ":0" was defined multiple times with different content (see the help page).
  5. ^ a b c d e f g h i "Anfibios del Ecuador". bioweb.bio. Retrieved 2022-10-13. Cite error: The named reference ":1" was defined multiple times with different content (see the help page).
  6. ^ Farrows. "Diablito". World Land Trust. Retrieved 2022-10-13.
  7. ^ a b c d Weygoldt, P. (2009-04-27). "Evolution of parental care in dart poison frogs (Amphibia: Anura: Dendrobatidae)". Journal of Zoological Systematics and Evolutionary Research. 25 (1): 51–67. doi:10.1111/j.1439-0469.1987.tb00913.x.
  8. ^ Myers, Charles W.; Daly, John W.; Malkin, Borys (1978). "A dangerously toxic new frog (Phyllobates) used by Emberá Indians of western Colombia, with discussion of blowgun fabrication and dart poisoning. Bulletin of the AMNH ; v. 161, article 2". {{cite journal}}: Cite journal requires |journal= (help)
  9. ^ Grant, Taran; Frost, Darrel R.; Caldwell, Janalee P.; Gagliardo, Ron; Haddad, Célio F. B.; Kok, Philippe J. R.; Means, D. Bruce; Noonan, Brice P.; Schargel, Walter E. (2006). PHYLOGENETIC SYSTEMATICS OF DART-POISON FROGS AND THEIR RELATIVES (AMPHIBIA: ATHESPHATANURA: DENDROBATIDAE). CENTRAL PARK WEST AT 79TH STREET, NEW YORK, NY 10024: BULLETIN OF THE AMERICAN MUSEUM OF NATURAL HISTORY. ISSN 0003-0090.{{cite book}}: CS1 maint: location (link)
  10. ^ a b Roland, Alexandre B.; Santos, Juan C.; Carriker, Bella C.; Caty, Stephanie N.; Tapia, Elicio E.; Coloma, Luis A.; O'Connell, Lauren A. (18 October 2017). "Radiation of the polymorphic Little Devil poison frog (Oophaga sylvatica) in Ecuador". Ecology and Evolution. 7 (22): 9750–9762. doi:10.1002/ece3.3503. ISSN 2045-7758. PMC 5696431. PMID 29188006.{{cite journal}}: CS1 maint: PMC format (link)
  11. ^ Pašukonis, Andrius; Serrano-Rojas, Shirley Jennifer; Fischer, Marie-Therese; Loretto, Matthias-Claudio; Shaykevich, Daniel A.; Rojas, Bibiana; Ringler, Max; Roland, Alexandre-Benoit; Marcillo-Lara, Alejandro; Ringler, Eva; Rodríguez, Camilo; Coloma, Luis A.; O’Connell, Lauren A. (2022-05-23). "Contrasting parental roles shape sex differences in poison frog space use but not navigational performance": 2022.05.21.492915. doi:10.1101/2022.05.21.492915. {{cite journal}}: Cite journal requires |journal= (help)
  12. ^ Rabeling, Christian; Sosa-Calvo, Jeffrey; O'Connell, Lauren A.; Coloma, Luis A.; Fernandez, Fernando (2016-09-19). "Lenomyrmex hoelldobleri: a new ant species discovered in the stomach of the dendrobatid poison frog, Oophaga sylvatica (Funkhouser)". ZooKeys. 618: 79–95. doi:10.3897/zookeys.618.9692. ISSN 1313-2970. PMC 5102051. PMID 27853401.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  13. ^ Moskowitz, Nora A.; Dorritie, Barbara; Fay, Tammy; Nieves, Olivia C.; Vidoudez, Charles; 2017 Biology Class, Cambridge Rindge Latin; 2017 Biotechnology Class, Masconomet; Fischer, Eva K.; Trauger, Sunia A.; Coloma, Luis A.; Donoso, David A.; O’Connell, Lauren A. (2020-01-01). "Land use impacts poison frog chemical defenses through changes in leaf litter ant communities". Neotropical Biodiversity. 6 (1): 75–87. doi:10.1080/23766808.2020.1744957.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  14. ^ McGugan, Jenna R.; Byrd, Gary D.; Roland, Alexandre B.; Caty, Stephanie N.; Kabir, Nisha; Tapia, Elicio E.; Trauger, Sunia A.; Coloma, Luis A.; O’Connell, Lauren A. (2016-06-01). "Ant and Mite Diversity Drives Toxin Variation in the Little Devil Poison Frog". Journal of Chemical Ecology. 42 (6): 537–551. doi:10.1007/s10886-016-0715-x. ISSN 1573-1561.
  15. ^ "Diablito". Reptipedia. Retrieved 2022-10-13.
  16. ^ a b c Farrows. "Diablito". World Land Trust. Retrieved 2022-10-13.
  17. ^ Lötters, S., Glaw, F., Köhler, J., and Castro, F. (1999). ''On the geographic variation of the advertisement call of Dendrobates histrionicus and related forms from north-western South America.'' Herpetozoa, 12(1/2), 23-38.
  18. ^ Santos, Juan C.; Baquero, Margarita; Barrio-Amorós, César; Coloma, Luis A.; Erdtmann, Luciana K.; Lima, Albertina P.; Cannatella, David C. (2014-12-07). "Aposematism increases acoustic diversification and speciation in poison frogs". Proceedings of the Royal Society B: Biological Sciences. 281 (1796): 20141761. doi:10.1098/rspb.2014.1761. PMC 4213648. PMID 25320164.{{cite journal}}: CS1 maint: PMC format (link)
  19. ^ Limerick, Sandra (1980). "Courtship Behavior and Oviposition of the Poison-Arrow Frog Dendrobates pumilio". Herpetologica. 36 (1): 69–71. ISSN 0018-0831.
  20. ^ "Dryad Data -- Warning signal brightness variation: sexual selection may work under the radar of natural selection in populations of a polytypic poison frog". doi:10.5061/dryad.p5g5j. {{cite journal}}: Cite journal requires |journal= (help)
  21. ^ Dreher, Corinna E.; Cummings, Molly E.; Pröhl, Heike (2015-06-25). "An Analysis of Predator Selection to Affect Aposematic Coloration in a Poison Frog Species". PLOS ONE. 10 (6): e0130571. doi:10.1371/journal.pone.0130571. ISSN 1932-6203. PMC 4481408. PMID 26110826.{{cite journal}}: CS1 maint: PMC format (link) CS1 maint: unflagged free DOI (link)
  22. ^ jlp342 (2018-03-21). "Chytridiomycosis". cwhl.vet.cornell.edu. Retrieved 2022-10-13.{{cite web}}: CS1 maint: numeric names: authors list (link)
  23. ^ Knight, Kathryn (2019). "How poison dart frogs export potent poisons to their skins". Journal of Experimental Biology. 222 (12): jeb207910. doi:10.1242/jeb.207910.
  24. ^ Moskowitz, Nora A.; Dorritie, Barbara; Fay, Tammy; Nieves, Olivia C.; Vidoudez, Charles; 2017 Biology Class, Cambridge Rindge Latin; 2017 Biotechnology Class, Masconomet; Fischer, Eva K.; Trauger, Sunia A.; Coloma, Luis A.; Donoso, David A. (2020-01-01). "Land use impacts poison frog chemical defenses through changes in leaf litter ant communities". Neotropical Biodiversity. 6 (1): 75–87. doi:10.1080/23766808.2020.1744957. S2CID 202846094.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  25. ^ Moskowitz, Nora A.; Dorritie, Barbara; Fay, Tammy; Nieves, Olivia C.; Vidoudez, Charles; 2017 Biology Class, Cambridge Rindge Latin; 2017 Biotechnology Class, Masconomet; Fischer, Eva K.; Trauger, Sunia A.; Coloma, Luis A.; Donoso, David A. (2020-01-01). "Land use impacts poison frog chemical defenses through changes in leaf litter ant communities". Neotropical Biodiversity. 6 (1): 75–87. doi:10.1080/23766808.2020.1744957. S2CID 202846094.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  26. ^ Moskowitz, Nora A.; Dorritie, Barbara; Fay, Tammy; Nieves, Olivia C.; Vidoudez, Charles; 2017 Biology Class, Cambridge Rindge Latin; 2017 Biotechnology Class, Masconomet; Fischer, Eva K.; Trauger, Sunia A.; Coloma, Luis A.; Donoso, David A. (2020-01-01). "Land use impacts poison frog chemical defenses through changes in leaf litter ant communities". Neotropical Biodiversity. 6 (1): 75–87. doi:10.1080/23766808.2020.1744957. S2CID 202846094.{{cite journal}}: CS1 maint: numeric names: authors list (link)
  27. ^ Daly, John W.; Spande, Thomas F.; Garraffo, H. Martin (2005-10-01). "Alkaloids from Amphibian Skin: A Tabulation of Over Eight-Hundred Compounds". Journal of Natural Products. 68 (10): 1556–1575. doi:10.1021/np0580560. ISSN 0163-3864.
  28. ^ a b c d Caty, Stephanie N.; Alvarez-Buylla, Aurora; Byrd, Gary D.; Vidoudez, Charles; Roland, Alexandre B.; Tapia, Elicio E.; Budnik, Bogdan; Trauger, Sunia A.; Coloma, Luis A.; O'Connell, Lauren A. (2019-01-01). "Molecular physiology of chemical defenses in a poison frog". Journal of Experimental Biology. doi:10.1242/jeb.204149. ISSN 1477-9145.
  29. ^ a b c d O'Connell, Lauren A.; O'Connell, Jeremy D.; Paulo, Joao A.; Trauger, Sunia A.; Gygi, Steven P.; Murray, Andrew W. (2021-02-01). "Rapid toxin sequestration modifies poison frog physiology". Journal of Experimental Biology. 224 (3). doi:10.1242/jeb.230342. ISSN 0022-0949. PMC 7888741. PMID 33408255.{{cite journal}}: CS1 maint: PMC format (link)
  30. ^ Fischer, Eva K.; Roland, Alexandre B.; Moskowitz, Nora A.; Vidoudez, Charles; Ranaivorazo, Ndimbintsoa; Tapia, Elicio E.; Trauger, Sunia A.; Vences, Miguel; Coloma, Luis A.; O’Connell, Lauren A. (2019-12-02). "Mechanisms of Convergent Egg Provisioning in Poison Frogs". Current Biology. 29 (23): 4145–4151.e3. doi:10.1016/j.cub.2019.10.032. ISSN 0960-9822. PMID 31761700.
  31. ^ Yen, Tien-Jui; Lolicato, Marco; Thomas-Tran, Rhiannon; Du Bois, J.; Minor, Daniel L. (2019-06-07). "Structure of the saxiphilin:saxitoxin (STX) complex reveals a convergent molecular recognition strategy for paralytic toxins". Science Advances. 5 (6): eaax2650. doi:10.1126/sciadv.aax2650. ISSN 2375-2548. PMC 6584486. PMID 31223657.{{cite journal}}: CS1 maint: PMC format (link)
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