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Heterochrony in Growth and Development in Anurans from the Chaco of South America

Abstract

Heterochrony refers to those permutations in timing of differentiation events, and those changes in rates of growth and development through which morphological changes and novelties originate during phyletic evolution. This research analyzes morphological variation during the ontogeny of 18 different anuran species that inhabit semi-arid environments of the Chaco in South America. I use field data, collection samples, and anatomical methods to compare larval growth, and sequences of ontogenetic events. Most species present a similar pattern of larval development, with a size at metamorphosis related to the duration of larval period, and disappearance and transformations of larval features that occur in a short period between forelimb emergence and tail loss. Among these 18 species, Pseudis paradoxa has giant tadpole and long larval development that are the results of deviations of rates of growth. In this species events of differentiation that usually occur at postmetamorphic stages have an offset when tail is still present. Tadpoles of Lepidobatrachus spp. reach large sizes at metamorphosis by accelerate developmental rates and exhibit an early onset of metamorphic features. The uniqueness of the ontogeny of Lepidobatrachus indicates that evolution of anuran larval development may occasionally involve mid-metamorphic morphologies conserving a free feeding tadpole and reduction of the morphological-ecological differences between tadpoles and adults.

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Acknowledgments

I am grateful to Natalia von Ellenrieder for many suggestions on the English written. Two anonymous reviewers contributed with many comments to improve the manuscript. Javier Goldberg, Silvia Quinzio, and Fernando Hongn provided many useful suggestions and comments. Fernando Hongn, Gladys Gonzo, Javier Goldberg, Silvia Quinzio, Roberto Bernal, and Soledad Valdecantos collaborated with field work. This research was supported Consejo Nacional de Investigaciones Científicas y Técnicas PIP 0239.

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Correspondence to Marissa Fabrezi.

Appendix

Appendix

Localities Studied

Localities in which larval development was studied are placed in the Chaco region that comprises a plain of approximately 1.141.000 km2 in the south-central South America (from 16° 55′ S–33° 52′ and 67° 50′W– 57° 52′W). It is an arid and subtropical region of low forests and savannas traversed by only two permanent rivers: Pilcomayo and Bermejo that flow southeastward across the plain from their Andean headwaters to Paraguay River. The Chaco is subject to climates that vary from tropical in the north to warm-temperate in the south. The mean of annual temperature varies between 26º and 16º with an average of 22°C. The highest recorded temperatures for the continent occur in the Chaco with absolute maximums that may reach 54°C. There is marked seasonality, with warm summers with precipitations ranging with a West-East gradient from 300 to 1,000 mm. Evaporation losses (1,500–900 mm) sharply reduce the effective precipitation and give the Chaco an arid nature that is absent only in the permanent swamps and forests along Paraguay River. Specimens and field data presented in this research were obtained from three localities:

Locality 1:

Totoralejos, Córdoba, Argentina: 29°38′28.00′′S, 64°50′58.37′′W. Taxa found in this locality at the same time (late December 2004; January 2006): Ceratophryidae (Chacophrys pierottii, Lepidobatrachus llanensis), Leptodactylidae (Leptodactylus mystacinus)

Locality 2:

Provincial Route 5, between 24°44′8.00′′S, 64°12′8.23′′W–24°26′9.17′′S, 63°59′17.62′′W. Taxa found in this locality during the four rainy seasons (November–April 1994–1997, 2007): Bufonidae (Rhinella arenarum, R. schneideri), Ceratophryidae (Ceratophrys cranwelli, Lepidobatrachus llanensis), Cycloramphidae (Odontophrynus lavillai), Hylidae (Phyllomedusa sauvagii, Scinax fuscovarius, S. nasicus, Trachycephalus typhonius), Leiuperidae (Physalemus biligonigerus, P. cuqui; Pleurodema tucumanum), Leptodactylidae (Leptodactylus chaquensis, L. bufonius, L. fuscus, L. latinasus, L. mystacinus), Microhylidae (Dermatonotus muelleri, Elachistocleis bicolor)

Locality 3:

National Route 81, between 23°12′34.68′′S, 63°34′27.48′′W–23°14′49.96′′S, 63°21′11.64 W. Species found in this locality during several rainy seasons (November–April, 1996–2010): Bufonidae (Rhinella granulosa, R. schneideri), Ceratophryidae (Ceratophrys cranwelli, Chacophrys pierottii, Lepidobatrachus laevis, L. llanensis), Hylidae (Dendropsophus nanus, Hypsiboas raniceps, Phyllomedusa azurea, P. sauvagii, Pseudis paradoxa, Scinax acuminatus, S. fuscovarius, S. nasicus, Trachycephalus typhonius), Leiuperidae (Physalemus biligonigerus, P. cuqui); Leptodactylidae (Leptodactylus chaquensis, L. bufonius, L. fuscus, L. latinasus, L. mystacinus), Microhylidae (Dermatonotus muelleri, Elachistocleis bicolor)

Geographical Ranges of Studied Species

Frost (2011) summarized the distribution of the studied species as follows:

Ceratophrys cranwelli: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Chacophrys pierottii: Chacoan region, Argentina, Paraguay, and Bolivia

Dermatonotus muelleri: Northern Argentina, eastern Bolivia; Paraguay; Brazil

Elachistocleis bicolor: Central Argentina and Uruguay, Paraguay, Bolivia and Amazonian Brazil.

Lepidobatrachus laevis:: Chacoan region, Argentina, Paraguay, and Bolivia

Lepidobatrachus llanensis: Chacoan region, Argentina, Paraguay, and Bolivia

Leptodactylus chaquensis: Chacoan region, Argentina, Bolivia, Paraguay and northern Uruguay, and southern Brazil.

Leptodactylus fuscus: Savannas from Panama throughout South America, east of the Andes, Brazil, Bolivia, Paraguay, and Argentina.

Leptodactylus latinasus: Chacoan region, Argentina, Bolivia, and Paraguay and Uruguay, and southern Brazil

Leptodactylus mystacinus: Bolivia, Brazil, Uruguay, Paraguay to central Argentina.

Phyllomedusa azurea: Chacoan region, Argentina, Paraguay, and Bolivia and pantanal and cerrado regions, Brazil with an isolated population in southern Brazil.

Phyllomedusa sauvagii: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Physalaemus biligonigerus: Northern and central Argentina; Bolivia; Paraguay; Uruguay; southern Brazil.

Pseudis paradoxa*: Lower Río Magdalena Valley as well as Arauca and Meta in Colombia; Guianas from northeastern Venezuela east through Guyana, Surinam, and French Guiana to the mouth of the Amazon, thence west in the Amazon Valley to northern Bolivia and southeastern Peru; Trinidad. * Populations in the northern of Argentina were recognized as Pseudis paradoxa by Garda et al. (2010).

Scinax acuminatus: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay

Scinax fuscovarius: Argentina, Bolivia, Brazil, and Paraguay, between 150 and 1,800 m elevation.

Scinax nasicus: Chacoan region, Argentina, Bolivia, Brazil, and Paraguay and central Argentina, Uruguay, and southern Brazil

Trachycephalus typhonius: Lowlands of tropical Mexico, Central America, Trinidad and Tobago, Amazon Basin, Paraguay, northern Argentina.

Specimens Examined

Analyses of external morphology, measurements, and whole mounts of skeleton and peripheral nerves were obtained from the following list of specimens that are deposited in the Museo de Ciencias Naturales, Universidad Nacional de Salta, Argentina (MCN).

Ceratophryidae

Chacophrys pierottii

Locality 1:

MCN 1027 (60 specimens, larval stages 26–31, January, 16 2006); MCN 1028 (40 specimens, larval stages 31–36, January, 22, 2006), MCN 1029 (56 specimens, larval stages 35–46, January, 28, 2006), MCN 987 (nine males, three females, December, 29, 2004), MCN 1045 (one female, January, 16, 2006)

Lepidobatrachus llanensis

Locality 1:

MCN 986 (six males, 3 females, December 29, 2004), MCN 1122 (14 specimens, larval stages 39–46, January 28, 2006), MCN 1178 (36 specimens, larval stages 32–38, January 16, 2006)

Locality 2:

MCN s/n, (14 specimens, larval stages 31–37, November 15, 1996), MCN s/n (3 specimens, larval stages 39–41, November 21, 1996)

Locality 3:

MCN 567 (55 specimens, larval stages 33–39, December 1, 1998), MCN 932 (43 specimens, larval stages 31–37, November 25, 2000), MCN 665 (70 specimens, larval stages 36–41, January 5, 2000), MCN 1118 (45 specimens, larval stages 36–46, December 18, 2005), MCN 1319/1321 (36 specimens, larval stages 39–46, December 9, 2009)

Lepidobatrachus laevis

Locality 3:

MCN 936 (one juvenile, November 2, 1998), MCN 663 (15 specimens, larval stages 36–41, December 1, 1998), MCN 647 (25 specimens, larval stages 33–40, January 5, 2000), MCN 666 (seven specimens, larval stages 38–43 and one froglet, January 5, 2000); MCN 668 (one froglet, January 5, 2000), MCN 695/696 (three juvenile specimen, January 5, 2000), MCN 934 (one juvenile, November 25, 2000), MCN 931 (three adults, January 20, 2001); MCN 935 (one juvenile, January 2003); MCN 815 (one adult and three juveniles, December 15, 2003), MCN 814 (six specimens, larval stages 36–38, December 28, 2003), MCN 817 (three juveniles, December 28, 2003), MCN 989 (one female, April 15, 2005), MCN 1175 (35 specimens, larval stages 34–46, December 18, 2005), MCN 1174 (female, March 10, 2006), MCN 1341 (two specimens, larval stages 39, December 27, 2008), MCN 1324 (seven froglets, February 7, 2009), MCN 1320/1322 (56 specimens, stages 39–46, December 8, 2009)

Ceratophrys cranwelli

Locality 2:

MCN 414 (38 specimens, larval stages 28–33, December 1, 1995), MCN 413 (22 specimens, larval stages 37–46, December 16, 1995); MCN 415 (24 specimens, larval stages 26–31, January 18, 1996), MCN 420 (13 specimens, larval stages 36–40, January 26, 1996), MCN 425 (seven specimens, larval stages 42–46, February 2, 1996), MCN 1345 (58 specimens, larval stages 26–36, December 1, 2007), MCN s/n (25 specimens, larval stages 39–44, December 12, 2007)

Locality 3:

MCN 1190 (23 specimens, larval stages 33–38, December 18, 2005); MCN 1034 (27 specimens, larval stages 37–43, March 23, 2006), MCN 1318 (14 specimens, larval stages 34–37, December 8, 2009)

Hylidae

Phyllomedusa azurea

Locality 3:

MCN 1054 (44 specimens, larval stages 34–40, February 10, 2005); MCN 1177 (78 specimens larval stages 33–44, April 1, 2006); MCN 1309 (66 specimens, larval stages 36–44, March 13, 2007); MCN 1326 (80 specimens larval stages 33–41, February 27, 2010); MCN 1346 (54 specimens, larval stages 37–46, April 14, 2010)

Phyllomedusa sauvagii

Locality 3:

MCN 1159 (76 specimens, larval stages 31–39, December 29, 2004); MCN 1077 (69 specimens, larval stages 33–42, February 17, 2005); MCN 1309 (103 specimens, larval stages 37–43, March 13, 2007); MCN 1348 (46 specimens larval stages 32–41, February 27, 2010); MCN 1330 (45 specimens, larval stages 38–46, April 04, 2010)

Pseudis paradoxa

Locality 3:

MCN 988 (35 specimens, larval stages 33–38, February 10, 2005); MCN 1171 (33 specimens, larval stages 33–42, March 10, 2006), MCN 1196 (54 specimens, larval stages 33–43, March 13, 2007); MCN 1197 (59 specimens, larval stages 33–46, April 4, 2007)

Scinax acuminatus

Locality 3:

MCN 1145 (48 specimens, larval stages 38–42, December 12, 2004); MCN 1339 (78 specimens, larval stages, 38–44, December 27, 2009); MCN 1347 (45 specimens, larval stages 37–46, April 14, 2010)

Scinax fuscovarius

Locality 3:

MCN 1134 (33 specimens, larval stages 34–38, November 2, 2001); MCN 1105 (43 specimens, larval stages 37–41, November 29, 2004); MCN 1144 (38 specimens, larval stages 38–44, December 29, 2004); MCN 1191 (60 specimens, larval stages 32–42, December 18, 2005); MCN 1315 (47 specimens, larval stages 38–46, January 05, 2008)

Scinax nasicus

Locality 3:

MCN 1350 (48 specimens, larval stages, 36–43, December 28, 2005); MCN 1349 (15 specimens, larval stages 37–44, December 30, 2006); MCN 1317 (53 specimens, larval stages 38–46, January 5, 2008)

Trachycephalus typhonius:

Locality 3:

MCN 1127 (49 specimens, larval stages 37–43, January 2, 2001); MCN 1337 (58 larval specimens, larval stages 37–42, December 27, 2007), MCN 1333 (33 specimens, larval stages 38–46, January 05, 2008)

Leiuperidae

Physalaemus biligonigerus

Locality 3:

MCN 1092 (45 specimens, larval stages 36–43, December 29, 2004); MCN 1097 (58 specimens, larval stages 37–46, February 17, 2005); MCN 1078 (35 specimens, larval stages 39–46, February 17, 2005), MCN 1079 (33 specimens, larval stages 38–42, March 12, 2005)

Leptodactylidae

Leptodactylus chaquensis

Locality 2:

MCN 1343 (56 specimens larval stages 35–37, December 1, 2007), MCN s/n (35 specimens, larval stages 40–42, December 12, 2007)

Locality 3:

MCN 1148 (78 specimens, larval stages 35–38, January 17, 2000); MCN 1335 (85 specimens, larval stages 39–44; 45, December 27, 2007)

Leptodactylus fuscus

Locality 2:

MCN 1344 (33 specimens, larval stages 39–43, December 1, 2007)

Locality 3:

MCN 816 (27 specimens, larval stages 38–42, December 28, 2003); MCN MCN 1089 (45 specimens, larval stages 39–43, December 29, 2004); 1336 (73 specimens, larval stages 39–44, December 27, 2007)

Leptodactylus mystacinus

Locality 3:

MCN 1351 (15 specimens, larval stages 39–46, December 30, 2006); MCN 1342 (25 specimens, larval stages 39–42, December 27, 2007)

Leptodactylus latinasus

Locality 3:

MCN 1126 (43 specimens, larval stages 37–42, February 10, 2005), MCN 1352 (140 specimens, larval stages 38–46, December 27, 2007)

Microhylidae

Dermatonotus muelleri

Locality 3:

MCN 1016 (60 specimens, larval stages 34–39, March 4; 2004); MCN 946 (55 specimens, larval stages 30–37, December 11, 2004); MCN 1094 (38 specimens, larval stages 38–43, December 29, 2004); MCN 997 (45 specimens, larval stages 31–37, February 9, 2005); MCN 1080 (23 specimens, larval stages 38–44, February 17, 2005), MCN s/n (100 specimens, larval stages 26–31, December 12, 2007), MCN 1340 (123 specimens, larval stages 35–39, December 27, 2007), MCN 1332 (75 specimens, larval stages 37–46, January 5, 2008)

Elachistocleis bicolor

Locality 3:

MCN 1164 (15 specimens, larval stages 37–42, January 17, 2000); MCN 1062 (22 specimens, larval stages 33–40, February 17, 2005); MCN 1081 (12 specimens, larval stages 32–37, March 12, 2005); MCN 1340 (5 specimens, larval stages 40–43, December 27, 2007)

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Fabrezi, M. Heterochrony in Growth and Development in Anurans from the Chaco of South America. Evol Biol 38, 390–411 (2011). https://doi.org/10.1007/s11692-011-9128-5

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Keywords

  • Tadpoles
  • Development
  • Metamorphosis
  • Growth
  • Anurans
  • Morphology