Dendropsophus ebraccatus

"Hourglass treefrog" redirects here. For other uses, see Hourglass treefrog (disambiguation).

Dendropsophus ebraccatus
In Panama
Conservation status
Least Concern (IUCN 3.1)
Scientific classification
Kingdom:	Animalia
Phylum:	Chordata
Class:	Amphibia
Order:	Anura
Family:	Hylidae
Genus:	Dendropsophus
Species:	D. ebraccatus
Binomial name
Dendropsophus ebraccatus (Cope, 1874)
Synonyms
Hyla weyerae Taylor, 1954 Hyla ebraccata

Dendropsophus ebraccatus, also known as the hourglass treefrog or pantless treefrog, is a neotropical treefrog, found scattered throughout Central and South America from southern Mexico to northern Ecuador. The common names of D. ebraccatus come from the dark hourglass shaped pattern found in the centre of the back and the distinct smooth yellow thighs that contrast the rest of the brazenly patterned body. The contrasting of the smooth yellow thighs from the rest of the bodies pattern provide the illusion that D. ebraccatus is not wearing pants. The name ebraccata in Latin means "without trousers". D. ebraccatus has a number of unique reproductive features, such as the ability to alter rates of hatching shared in a number of Anura families. D. ebraccatus is also unique in its ability to alter its mode of reproduction as it is the only known vertebrate to be able to do so.

Taxonomy

Dendropsophus ebraccatus is a member of the wide-ranging tree frog family Hylidae and the genus Dendropsophus. Dendropsophus is a group of small, primarily yellow tree frogs found in dense jungles throughout Central and South America. A unique feature of the genus is that all individuals within the genus have 30 chromosomes. After a large revision to the family Hylidae following (Faivovich et al. 2005) the genus Dendropsophus was revived and separated from Hyla.

Distribution and habitat

The hourglass tree frog is native to southern Mexico, Belize, Colombia, Costa Rica, Ecuador, Guatemala, Honduras, Nicaragua, Panama, western Colombia, and northwestern Ecuador. They can be found in terrestrial and freshwater habitats, usually under the canopy of tropical rainforests, and prefer temperature ranges of 74-76 °F with moderately high humidity between 60-70%. It has an upper elevation limit of 1,600 metres

Physiology

These frogs are smooth, small treefrogs exhibiting sexual dimorphism, males being significantly smaller than females. Their dorsal coloration consists of an hourglass pattern on their backs with gold spots in this pattern. This pattern varies from bright yellow-green to pale yellow or cream. They are also called “pantless frogs”. When you extend their hind legs you can see that only on their thighs they do not have the pattern continued but rather just a pale yellow color. The hourglass tree frog has relatively large forelimbs compared to the proportion of its body. It also has well developed toe discs for tree climbing. Their toe pads adhere via deformation of the soft epithelial cells. They also have long hind limbs for jumping from tree to tree (Touchon and Warkentin 2008) [10]. As compared to most Anura they are capable of gas exchange through their permeable skin.

The frog family Hylidae has the unique adaptation of forming cocoons by shedding the outer skin layer of the stratum corneu. They also seek refuge in tree holes to protect themselves from desiccation during unfavorable conditions. They also secrete a watery mucus to aid in evaporative cooling. Their granular glands contain a wide range of bioactive molecules for defense. Compounds such as alkaloids, quinones, steroids, biogenic amines and a diversity of biologically active peptides can be found across the family Hylidae.

Adults are nocturnal creatures, their diet consists of small arthropods. While tadpoles are macrophagous herbivores, but may display cannibalistic behavior in the presence of dead tadpoles (Cope 1874)[4]. They can make loud calls due to the elasticity of their throats. Their call is a prolonged “creek” followed by several higher pitched “eeks”. They emit rain calls in the daytime before or during a rain shower.

Reproduction

Hourglass tree frogs migrate to freshwater pools in vegetated areas to breed during the rainy seasons of Central and South America, between May and November [13]. Once aggregated around freshwater pools, they utilize chorus and mate finding strategies to select mates. Males hide behind foliage around edges of marshes and ponds during the night and produce long mating calls to attract potential female mates. Once a male is selected by a female, he will climb onto her back and release his sperm into her cloaca.

Females reproduce multiple times within the breeding season, with gaps between reproductive spells as short as 10 days. Females will lay between 180 and 300 eggs, separated between up to eight different masses within a single night [13]. Egg masses are laid either in single layers on the upper surface of leaves overhanging freshwater or in clusters connected to floating vegetation within the water itself, depending on various environmental factors. Hourglass tree frogs are unique in their reproductive plasticity, allowing them to produce both aquatic and arboreal eggs. Arboreal eggs are deposited on the upper surfaces of leaves overhanging water, so the tadpoles can roll into the water once hatched, and aquatic eggs are attached to floating vegetation within the water to keep the eggs from sinking. If there is a risk of egg desiccation, eggs will be placed in the hydrating water, but if there is a risk of egg predation from fish in freshwater pools, eggs will be placed on leaves [13]. The threat of aquatic predation has been shown to outway the risk of desiccation. Undisturbed Aquatic eggs develop at a slightly faster rate than arboreal eggs with an average hatch time of 3.5 days after placement. Both egg groups can alter their rate of development in the presence of unfavourable conditions such as weather or predation. Rates of development and hatching time can be altered from 67% faster to 600% slower than undisturbed hatch times [13]. The rate of development is partially controlled by the rate of enzyme secretion by the hatching gland within the egg. The enzymes secreted by the hatching gland control the rate at which the eggs gel membrane is degradation [8].

Once eggs hatch, tadpoles either emerge in the water or roll off leaves into the pond below. Tadpoles are brown and gold with black eye bands and develop bright red tail colours in the presence of predators. Tadpoles feed on micro fauna and scavenge what they can in the water until they mature after 6–8 weeks. Young frogs live near pools of water and only make their way back to the forest canopy when nearing adulthood.

Conservation

The IUCN Red List of Threatened Species listed the Hourglass Tree Frog as a species of least concern (LC) in 2010 due to wide distribution, stable, large population, and high tolerance to adapt to habitat modifications. This species population is in many protected areas throughout the range. Although it is very adaptable it still faces many threats such as deforestation, agriculture and aquaculture (livestock farming and ranching, annual and perennial non-timber crops), logging, residential and commercial development, the pet industry, and pollution.

Research

The skin of the family Hylidae is vastly studied due to its rich sources of bioactive peptides, which has spiked the interest for drug development (Conlon 2014) [2]. Hylids use the peptides in defense against bacteria, fungi, protozoans, viruses, and desiccation (Conlon 2014) [2]. These peptides are of interest to scientist due to their anti-infective and therapeutic potential. Peptides have been found to stimulate insulin release for Type 2 diabetes mellitus therapy (Conlon 2014) [2]. They are also used for their ability to be the precursor for encoding cDNAs (Konig 2012) [6]. Pathogenic bacteria and fungi antibiotic resistance constitutes a serious threat to public health worldwide, scientists are looking to frogs skin secretions for further drug advancements (Conlon 2014) [2]

Mating

Mate Searching Behavior

Research on anuran communication reveals that groups of male frog chorus attract female frogs to mate. The relative success of these male frogs, including D. ebraccatus males, at attracting females depends on how their advertisement call is able to lead females to their calling space. As male density increases, a male’s advertisement call is confused with the other calls. This confusion leads to females’ inability to find which calling space the advertisement call originated from. The lowest intensity of a neighbor's call that a male frog is tolerant of is known as the aggressive threshold. When this threshold is reached, a male frog will use a different call known as an aggressive call to initiate male-male conflict or intolerance. Advertisement and aggressive calls both consist of an introductory note ending with a wide range of a number of clicks, and multiple notes and patterns.

Opposed to advertisement calls, aggression calls are characterized by a higher rate of repetition and longer timed calls.

Male/male Interactions

In opposition to most frog chorus species, D. Ebraccatus chorus groups produce far-range aggressive calls more frequently than close-range. The higher proportion and number of far-range aggression calls causes D. Ebraccatus males to be influenced by various surrounding calls in chorus groups instead of just calls from individual frogs. This influence from other males versus producing calls that attract females forces these male frogs to constantly adjust their calls accordingly. Generally, male frogs will respond to 2-4 Hz calls with synchronous advertisement calls. On the flip side, males will produce alternating advertisement calls or an initial delayed aggressive call when responding to a call that is 100 dB or more.

For aggressive calls, long calls are utilized for close interactions and physical altercations. During close interactions in which a male frog attacks another, they tussle with each other while still exchanging long duration calls. These physical alterations usually only last one minute unless they remain in close contact and will sometimes continue. On the other hand, short calls are utilized during far-range interactions.

Female/Male Interactions

Mate Choice

Call timing plays a role in female D. Ebraccatus mating choice. Although simultaneous male advertisement calling produces less reproductive success for males in close proximity, a male that starts its calls later is the preferred mating choice. This is because females seem to prefer calls that end last. Click notes at the end of the late advertisement call may be one reason why females prefer the late call since the clicking of the lead call is blocked by the late call.

The timing of male calls only depends on the call they produce and not the one they hear.  D. Ebraccatus males show more synchrony, or overlapping calls, when producing advertisement calls and prefer to alternate with other calls when they produce aggressive calls. Calls with 150 to 200 millisecond introductory note durations produced synchronous response calls the most efficiently. Although females generally prefer the late call, they are more attracted to the late call with the general timing of an advertising call being produced first and last. In cases where the lead male switches to aggressive calling (which is introduced in the courting section), the increased overlap between the lead aggressive call and the late advertisement call can cause females to not prefer the late advertisement call anymore.

Another aspect of male calls that influences mating choice is the number of notes. Many times, a responding advertisement call is synchronized to the first advertisement call as explained before but is also multi-noted. The advertisement calls are only 1-noted if in very dense choruses.

Courting

D. ebraccatus males produce calls in order to attract and court females leading to mating. There are two types of timed calls males produce: lead calls, which start first, and late or lagging calls, which start in the middle of the lead call. The timing of late calling males forces their male competitors to finish calling in the middle of their own advertisement call. This means the late caller finishes the call with its competitor calls being heard at the same time. In response to late male callers, the leading male callers adapted a strategy using aggressive calling. Since aggressive calling is longer than advertisement calling, the lead male switches to an aggressive call while the lagging male uses an advertisement call, which allows the lead male to finish last in more cases and increase their reproductive success. This strategy is an explanation for why D. ebraccatus have high levels of aggressive calls that would be costly for any other species of chorus frog mentioned in the male/male interactions subsection.

Despite this, the late call males cannot lengthen their time delay to decrease overlap and ensure that they finish last. The response time from one male call to another remains around 210 milliseconds no matter what call type they are producing or responding to besides the break increasing when male frogs switch to aggressive calling. There is also evidence that male frogs make many errors in aggressive call detection leading to decreased response time of a threat and decreased attraction by females since the call timing is off. Because females are more attracted to low aggression calls and advertisement calls, this could explain why male frogs are more likely to coordinate their levels of aggression to other calls. This is opposed to simply increasing the intensity of aggression in their call in response to other aggression calls.

The multi-noted synchronized call has two advantages: multiple notes can hide click notes in the leading call and synchronizing decreases the chance of the leader producing a call response. The decreased chance of a call response happens since many frogs will not answer if a call is produced less than 210 milliseconds after their first call has started. The only time a synchronous advertisement call is not multi-noted is in very dense choruses where advertisement calls are only 1-noted.

Social Behavior

Adult Sociality

Male aggressive calling not only is affected by mating and their need to defend their calling space but is also affected by social communication and environment with other aggressive males. In particular, the social environment surrounding a male responding to an intruder will affect the intensity of the responding aggressive calls produced. This idea of a social environment affecting aggressive call output started in this frog species with research examining the relationship between aggressive call intensity in response to an intruder versus their surrounding male competitors. With that being said, the effect of the social environment is much more complicated than that. Aggressive calls between males are not always from one individual to another. [8] In many cases, a call can be received by multiple frogs that must all compete to produce a responding call signal that is heard by the original frog. This finding means that D. ebraccatus males compete on many fronts during chorusing. They compete to find the best territory for producing calls that are heard over their competitors and for space where they themselves can receive calls. However, they can also compete to produce calls that are heard over others by adjusting their own call intensity in respect to surrounding aggressive calls. Males increase the aggressiveness of their calls when they have more competitors and when the aggressiveness of surrounding stimuli increases. Males decrease aggressive call intensity when there are a fewer number of competitors (or stimuli) and when surrounding calls have lower levels of aggressiveness.

Group Living

The common night call pattern of male chorus frog species is initially high aggressive call levels followed by a “stable chorus” with little to no aggressive calling. This pattern is due to habituation, the increase of aggressive thresholds in response to repeated calls greater than their original threshold. In contrast with most frog chorus species, a large fraction of D. ebraccatus males still make aggressive calls throughout the night with only a slight decrease. The continued aggressive calls throughout the night in this species indicates that D. ebraccatus males do not habituate in response to aggressive calls and instead are sensitized. In other words, these frogs initially decrease their aggressive threshold after exposure to repeated calls above threshold. This mechanism leads to more frequent aggressive calls than other chorus frogs. Anuran species that display chorus behaviors use aggressive calls as a mechanism to defend territory from other males, so it was not known for a while why high calling rates that expose male hourglass tree frogs to dangerous situations is maintained.

One possible reason for high aggressive calling levels is that D. ebraccatus aggressive and advertisement thresholds are initially equal, and they need to decrease their aggressive threshold in order to be able to distinguish and respond to these distinct call types. Generally, there is a 210 millisecond response time frame that males take to respond to one call with a call of their own. The only exception to this 210 millisecond time frame is when male frogs are making the decision to switch to aggressive calls. The male frogs seem to respond with their first aggressive call more slowly due to trying to distinguish an advertisement call from an aggressive call. Another reason for the higher aggressive calls in comparison with other chorus frogs is due to lead males adopting an aggressive call as a strategy to increase its attractiveness to females. This strategy is explained more in the mate choice subsection.

Another anomaly seen with D. ebraccatus males compared to other species is that their aggressive calls more often than not have intended recipients spanning far distances. These frequent far range aggressive calls in large chorus groups cause D. ebraccatus males to be influenced by various surrounding calls more often than calls from individual frogs. This influence from other males versus producing calls that attract females forces these male frogs to constantly adjust their calls accordingly.

Enemies

D. ebraccatus males will respond and synchronize with calls that are of similar frequency and length of different frog species. During instances in which there is male H. microcephala introductory note overlap with a male D. ebraccatus call, female D. ebraccatus frogs are less attracted to the D. ebraccatus male that produced that overlapping call. By having the ability to respond to similar calls of different species, the male D. ebraccatus is able to synchronize its calls to avoid introductory note overlap with the H. microcephala, thereby increasing females' attraction to the male once again.

Like advertisement calls, the male D. ebraccatus is able to respond to aggressive calls of other species. Like the overlap and confusion that happens within their own male species during mating calls, the same can happen between male D. ebraccatus and choruses of other species in close proximity like the H. microcephala and H. phleboes. Communication between these males allows for hostile interactions to take place and for calling space boundaries to be set.

References

1. Castanho L.M. 2001. Moulting Behaviour in Leaf-Frogs of the Genus Phyllomedusa (Anura: Hylidae). Zoologischer Anzeiger - A journal of Comparative ZoologyEcology and Behaviour. 240: 3-6. https://doi.org/10.1078/0044-5231-0000122. Conlon J.M., mechkarsha M., Lukic M.L., Flatt P.R. 2014. Potential therapeutic applications of multifunctional host-defense peptides from frog skin as anti-cancer, anti-viral, immunomodulatory, and anti-diavetic agents. Elsevier: Peptides 57: 67-77. https://doi.org/10.1016/j.peptides.2014.04.019.
2. Cohen, K.L., Piacentino, M.L., Warkentin M.K., 2018. The hatching process and mechanisms of adaptive hatching acceleration in hourglass treefrogs, Dendropsophus ebraccatus: Comparative Biochemistry and Physiology Part A: Molecular & Integrative Physiology. 217: 63-74.
3. Cope, E.D. 1874. Description of some species of reptiles obtained by Dr. John F. Bransford, Assistant Surgeon United States Navy, while attached to the Nicaraguan surveying expedition in 1873. Proceedings of the Academy of Natural Sciences of Philadelphia: 69.
4. Dendropsophus Ebraccatus Code 1874. Amphibians of Panama. 2018. http://biogeodb.stri.si.edu/amphibians/es/species/81/
5. Duellman, W.E. 2001. The Hylid Frogs of Middle America. Society for the Study of Amphibians and Reptiles, Ithaca, New York, USA.
6. Konig E., Clark V., Shaw C., Bininda-Emonds O.R.P. 2012. Molecular cloning of skin peptide precursor-encoding cDNAs from tibial gland secretion of the Giant Moneky Frog, Phyllomedusa bicolor (Hylidae, Anura). Elsevier: Peptides 38: 371-376. http://dx.doi.org/10.1016/j.peptides.2012.09.010.
7. OHMER, M.E. & Zamudio K.R., 2009. Discordance in body size, colour pattern, and advertisement call across genetically distinct populations in a Neotropical anuran (Dendropsophus ebraccatus): Biological Journal of the Linnean Society, 97, 298–313.
8. Powell R., Conant R., Collins J.T. 2016. Peterson Field Guide to Reptiles and Amphibians of Eastern and Central North America. Boston (NY): Houghton Mifflin Harcourt. 4: 494.
9. Touchon, J.C. & Warkentin, K.M., 2008. Reproductive mode plasticity: aquatic and terrestrial oviposition in a treefrog. Proceedings of the National Academy of Sciences of the United States of America, 105(21): 7495–9.
10. Touchon, J.C., & Worley J.L., 2015. Oviposition site choice under conflicting risks demonstrates that aquatic predators drive terrestrial egg-laying: Proceedings of the Royal Society B. 282 (1808): 0962-8452