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Neoichnology of the eastern spadefoot toad, Scaphiopus holbrookii (Anura: Scaphiopodidae): criteria for recognizing anuran burrows in the fossil record

Lauren M. Johnson and Daniel I. Hembree

Plain Language Abstract

Frogs and toads first appear in the fossil record approximately 190 million years ago. Although terrestrial frogs and toads are considered have evolved first, their early record is less understood than that of aquatic groups. Many living terrestrial frogs and toads construct burrows to escape extreme temperatures, dry conditions, or predators. Fossil burrows may, therefore, be used to suggest the presence of these animals if they can be recognized. Unfortunately the burrows of living frogs and toads are poorly understood. The eastern spadefoot toad, Scaphiopus holbrookii, belongs to one of four groups of burrowing terrestrial frogs and toads. This study describes the burrowing behaviors of S. holbrookii as well as the form and dimensions of their burrows produced in laboratory experiments with different types of soil. The toads used their rear legs to dig their burrows and moved very little soil to the surface. Three distinct types of burrows were produced: isolated chambers, vertical burrows with chambers, and subvertical burrows with chambers. In addition, the dimensions of the burrow chambers were similar to the toads, and distinct impressions on the burrow walls were produced by the toad's hind limbs and feet. The different types of burrows were produced consistently among the toads and the experiments. The dimensions of the different toad burrows were compared to each other and to burrows of scorpions, salamanders, and skinks. Spadefoot toad burrows were found to be similar to each other and different from those of the other animals. The results of this study will assist in the discovery of frog and toad burrows in the fossil record by providing a model for comparison. Application of this information will improve our understanding of the evolution of frogs and toads, their behavior, and the environments they have inhabited.

Resumen en Español

Neoichnología del sapo de espuelas del este, Scaphiopus holbrookii (Anura: Scaphiopodidae): criterios para el reconocimiento de las madrigueras de anuros en el registro fósil

Los anuros aparecen por primera vez en el Jurásico temprano, y aunque los anuros terrestres son considerados ancestrales, su registro más temprano es menos conocido que el de las formas acuáticas. Muchos anuros terrestres actuales producen madrigueras para escapar de las condiciones ambientales desfavorables. Las madrigueras fósiles de anuros podrían, por lo tanto, servir como evidencias de la presencia de anuros si su morfología es conocida. El sapo de espuelas del este, Scaphiopus holbrookii (Anura: Scaphiopodidae), pertenece a uno de los cuatro grupos de anuros terrestres que producen madrigueras. Este estudio describe los comportamientos de madriguera de S. holbrookii así como la morfología cualitativa y cuantitativa de sus madrigueras producidas en los experimentos de laboratorio con diferentes condiciones de sedimento. Los sapos utilizaron una primera técnica de madriguera con el uso del miembro posterior para mover una cantidad mínima de sedimentos hacia la superficie. Se produjeron tres arquitecturas distintas: cámaras ovoides aisladas, pozos verticales con cámaras ovoides, y ejes subverticales con cámaras ovoides. Las formas y los tamaños de las cámaras de la madriguera eran similares a las del sapo ocupante. Las impresiones en las paredes de la madriguera fueron producidas por las patas traseras y los pies de los sapos. La morfología cualitativa de la madriguera fue consistente entre los diversos individuos y experimentos. Las propiedades cuantitativas de las madrigueras de los sapos se compararon estadísticamente entre sí y con madrigueras de escorpiones, salamandras y lagartijas. Las madrigueras del sapo de espuelas eran similares entre sí y diferentes de las de los otros animales. Los resultados de este estudio ayudarán en la identificación de las madrigueras de anuros en el registro fósil, proporcionando un análogo para la comparación. La aplicación de estos datos puede mejorar la comprensión de la evolución de los anuros terrestres, su comportamiento, y su importancia paleoambiental.

Palabras clave: icnología; traza fósil; anuros; anfibio; continental; paleoecología

Traducción: Enrique Peñalver

Résumé en Français

Néo-ichnologie du crapaud pied-en-bêche oriental, Scaphiopus holbrookii (Anura : Scaphiopodidae) : critères de reconnaissance des terriers d'anoures dans le registre fossile

Les anoures apparaissent au Jurassique ancien, et bien que les anoures terrestres soient considérés comme étant ancestraux, leur registre fossile est moins bien compris que celui des formes aquatiques. De nombreux anoures terrestres actuels creusent des terriers pour se soustraire à des conditions environnementales défavorables. Des terriers fossiles pourraient donc témoigner de la présence d'anoures si leur morphologie était connue. Le crapaud pied-en-bêche oriental, Scaphiopus holbrookii (Anura : Scaphiopodidae), appartient à l'un des quatre groupes d'anoures terrestres qui creusent des terriers. Cette étude décrit les comportements de fouissage de S. holbrooki, ainsi que les propriétés qualitatives et quantitatives de la morphologie de leurs terriers creusés dans des sédiments variés, dans le cadre d'expériences en laboratoire. Les crapauds ont adopté une technique de fouissage utilisant d'abord les membres postérieurs, déplaçant une quantité minimale de sédiment à la surface. Trois types distincts d'architectures de terriers ont été produits : des chambres ovoïdes isolées, des conduits verticaux avec des chambres ovoïdes, et des conduits quasi-verticaux avec des chambres ovoïdes. Les formes et les tailles des chambres des terriers étaient similaires à celles des crapauds les occupant. Des empreintes sur les murs des terriers ont été laissées par les membres postérieurs et les pieds des crapauds. Les propriétés qualitatives de la morphologie des terriers sont restées constantes quels qu'aient été les individus et les expériences concernés. Les propriétés quantitatives des terriers de crapauds ont été comparées statistiquement les unes aux autres et avec celles des terriers de scorpions, de salamandres, et de lézards scinques. Les terriers des crapauds pieds-en-bêche sont similaires les uns aux autres et diffèrent de ceux des autres animaux. Les résultats de cette étude aideront à identifier les terriers d'anoures dans le registre fossile en leur fournissant un analogue actuel. L'utilisation de ces données permettra de mieux comprendre l'évolution des anoures terrestres, leur comportement, et leur importance en tant qu'indicateurs paléoenvironnementaux.

Mots-clés : ichnologie ; trace fossile ; anoure ; amphibien ; continental ; paléoécologie

Translator: Antoine Souron

Deutsche Zusammenfassung

Neoichnologie des Östlichen Schaufelfußes, Scaphiopus holbrookii (Anura: Scaphiopodidae): Kriterien für das Erkennen von Froschlurch-Bauten im Fossilrekord

Froschlurche tauchen erstmals im frühen Jura auf und obwohl terrestrische Anura als die Vorfahren gelten, ist ihre frühe Entwicklungsgeschichte weniger erforscht als die der aquatischen Formen. Viele heute lebenden terrestrischen Anura fertigen Erdbauten an, um ungünstigen Umweltbedingungen zu entkommen. Fossile Froschlurch-Bauten könnten daher als Proxy für die Anwesenheit von Anura fungieren, falls deren Morphologie bekannt wäre. Der Östliche Schaufelfuß, Scaphiopus holbrookii (Anura: Scaphiopodidae), gehört zu einer der vier Gruppen grabender terrestrischer Anura. Diese Untersuchung beschreibt das Grabverhalten von S. holbrookii ebenso wie die qualitative und quantitative Morphologie seiner Bauten, die unter Laborkonditionen mit verschiedenen Sedimentkonditionen entstanden. Die Kröten wandten eine Technik an, bei der sie zuerst das Hinterbein benutzten und eine kleine Menge Sediment an die Oberfläche bewegten. Es wurden drei unterscheidbare Architekturen produziert: isoliert, ovoide Kammern, vertikale Schäfte mit ovoiden Kammern und subvertikale Schäfte mit ovoiden Kammern. Die Form und die Größe der Kammern ähnelten der jeweiligen, den Bau belegenden Kröte. Abdrücke an den Wänden wurden hervorgerufen durch die Hinterbeine und Füße der Kröten. Die qualitative Morphologie war konsistent zwischen Individuen und Experimenten. Die quantitativen Merkmale der Kröten-Bauten wurden statistisch miteinander und mit Bauten von Skorpionen, Salamandern und Skinken verglichen. Die Schaufelfußkröten-Bauten waren sich untereinander ähnlich, unterschieden sich aber von denen anderer Tiere. Das Ergebnis dieser Untersuchung wird die Identifizierung von Froschlurch-Bauten im Fossilrekord durch ein Analogon zum Vergleichen unterstützen. Die Anwendung dieser Daten kann zum Verständnis der Evolution der terrestrischen Anura, ihrem Verhalten und ihrer Bedeutung für die Paläoumwelt beitragen.

Schlüsselwörter: Ichnologie; Spurenfossil; Froschlurche; Amphibie; kontinental; Paläoökologie

Translator: Eva Gebauer

Arabic

558 arab

Translator: Ashraf M.T. Elewa

 

 

TABLE 1. Experimental parameters, the number of burrows produced in each experiment, and the distribution of burrow architecture among experiments. Terrarium size is in gallons. Sediment moisture values are in percent total volume. Duration is in days. Burrow architectures: IC = isolated chamber; VS = vertical shaft with terminal chamber; SS = subvertical shaft with terminal chamber. (All six tables presented in one PDF file.)

TABLE 2. Quantitative measurements of vertical shafts . All measurements in cm or degrees (slope only). SH# = Scaphiopus holbrookii burrow cast identification number. Sediment: O = 100% organic coconut fiber; LOS = layered 100% organic coconut fiber and sand; MOS = homogenized mixture of 100% organic coconut fiber and sand. (All six tables presented in one PDF file.)

TABLE 3. Quantitative measurements of subvertical shafts . Refer to Table 2 caption for legend. (All six tables presented in one PDF file.)

TABLE 4. Quantitative measurements of isolated chambers . Refer to Table 2 caption for legend. (All six tables presented in one PDF file.)

TABLE 5. Width and height of each toad compared to mean width and height values of the terminal chambers produced by each toad. All measurements are in cm. (All six tables presented in one PDF file.)

TABLE 6. Properties of dwelling traces (VS and SS) and a single resting trace (SHT16). Burrow architectures: VS = vertical shaft with terminal chamber; SS = subvertical shaft with terminal chamber; RT = resting trace. (All six tables presented in one PDF file.)

 

APPENDIX 1.

Video of Scaphiopus holbrookii burrowing in an organic-rich sediment. Click on image to run animation.

animation 

APPENDIX 2.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results (p values) from the comparison of burrow properties in each of the clusters generated when comparing burrows of Scaphiopus holbrookii (see Figure 8). 1, Burrows in Cluster 1 compared to those in Clusters 2-4. 2, Burrows in Cluster 2 compared to those in Clusters 3 and 4. 3, Burrows in Cluster 3 compared to those in Cluster 4. Highlighted values in the upper tables indicate statistical difference (p < 0.05). Mean, median, standard deviation, and range are given in the lower tables for burrow properties that are statistically different. Highlighted values of properties in the lower tables are the greater of the two. Electronic file available.

APPENDIX 3.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results ( p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii and Pandinus imperator (see Figure 10). 1, All burrows produced by S. holbrookii compared to all burrows produced by P. imperator. 2, Burrows in Cluster A compared to those in Cluster B. See Appendix 2 caption for further table description. Electronic file available.

APPENDIX 4.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results ( p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii and Mabuya multifasciata (see Figure 11) . 1, All burrows produced by S. holbrookii compared to all burrows produced by M. multifasciata. 2, Burrows in Cluster A compared to those in Clusters B and C. 3, Burrows in Cluster B compared to those of Cluster C. See Appendix 2 caption for further table description. Electronic file available.

APPENDIX 5.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results ( p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii and Ambystoma tigrinum (see Figure 12). 1, All burrows produced by S. holbrookii compared to all burrows produced by A. tigrinum. 2, Burrows in Clusters A, B, C and D compared to those in Cluster E. 3, Burrows in Cluster A compared to those in Clusters B, C, and D. 4, Burrows in Cluster B compared to those in Clusters C and D. 5, Burrows in Cluster C compared to those in Cluster D. See Appendix 2 caption for further table description. Electronic file available.

APPENDIX 6.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results ( p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii, Pandinus imperator, Mabuya multifasciata, and Ambystoma tigrinum (see Figure 13). 1, Burrows in Cluster A compared to those in Clusters B, C, D, E, and F. 2, Burrows in clusters B and C compared to those in E and F. 3, Burrows in Clusters B and C compared to those in Cluster D. 4, Burrows in Cluster B compared to those in Cluster C. 5, Burrows in Cluster E compared to those in Cluster F. See Appendix 2 caption for further table description. Electronic file available.

APPENDIX 7.

Burrow properties and the resulting mean, median, standard deviation, maximum, minimum, and range values for individual clusters generated when comparing properties of burrows produced by Scaphiopus holbrookii, Pandinus imperator, Mabuya multifasciata, and Ambystoma tigrinum (See Figure 13). 1, Cluster A. 2, Cluster B. 3, Cluster C. 4, Cluster D. 5, Cluster E. 6, Cluster F. Highlighted values indicate burrow properties that are similar within an individual cluster based on standard deviation and range. Electronic file available.

APPENDIX 8.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results (p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii in varying sediment compositions. Highlighted values indicate statistical difference (p < 0.05). O = 100% organic coconut fiber, LOS = layered 100% organic coconut fiber and sand, MOS = homogenized mixture of 100% organic coconut fiber and sand. Electronic file available.

APPENDIX 9.

Mann-Whitney (MW) and Kolmogorov-Smirnov (KS) test results (p values) from the comparison of the properties of burrows produced by Scaphiopus holbrookii during 10-14 day and 30-40 day trials. Highlighted values indicate statistical differences (p < 0.05). Electronic file available.

 

 

FIGURE 1. Anuran morphology. 1, Basic anuran anatomy. Inset picture shows an enlarged hindlimb with tubercles located on the base of the pes. 2, Scaphiopus holbrookii on the sediment surface. 3, S. holbrookii burrowing beneath the surface.

 figure 1

FIGURE 2. Quantitative properties of burrows. 1, Measured properties include maximum depth (D), tunnel and shaft width (w), height (h), and circumference (c), length (L), and slope (S). 2, Complexity (C) is the sum of the number of surface openings (e), segments (s), and chambers (h) of a burrow. 3, Tortuosity is a measure of the average sinuosity of all of the segments of a burrow system. The tortuosity of a single segment is calculated by dividing the length (u) by the straight-line distance (v). Modified from Hembree et al. (2012).

figure 2 

FIGURE 3. Surface feature produced by Scaphiopus holbrookii. 1, Shallow pit in the sediment surface. 2, Two separate, closely spaced burrow openings. 3, A single circular burrowing opening. 4, Excavated sediment (sand) on top of a burrow opening.

figure 3 

FIGURE 4. Bioglyphs produced during burrow construction. 1-2, Photo (1) and line drawing (2) of a raised ridge on the bottom of the terminal chamber (SH11). The arrows in 1 and 2 and circled area in 2 indicate the position of the ridge on the base of the chamber. 3-4, Photo (3) and line drawing (4) of an imprint of an individual’s hind limb (SH11). The arrows in 3 and 4 and circled area in 4 indicate the position of the imprint on the chamber floor. 5-6, Photo (5) and line drawing (6) of a terminal chamber showing multiple triangular protrusions (SH25). The arrows in 5 and 6 and circled areas in 6 indicate the positions of the protrusions on the chamber walls.

figure 4 

FIGURE 5. Vertical shafts with terminal chambers1, Side view (SH25). 2, Frontal view (SH33). 3, Side view (SH33).

figure 5 

FIGURE 6. Subvertical shafts with terminal chambers. 1, View from the back of burrow (SH11). 2, Side view (SH11). 3, Side view (SH14).

figure 6 

FIGURE 7. Isolated chambers. 1, Side view (SH20). 2, Frontal view (SH20). 3, Frontal view (SH67).

 figure 7

FIGURE 8. Cluster analysis of all burrows produced by Scaphiopus holbrookii. Numbers in yellow circles indicate a major cluster of burrows discussed in the text. The color of the burrow specimen number indicates the architecture of the burrow: red = vertical shafts; orange = subvertical shafts; green = isolated chambers. The similarity values of the clusters are indicated by an arrow and a number. RT = resting trace.

figure 8 

FIGURE 9. Three different species and their respective burrows produced in previous studies. 1, An emperor scorpion (Pandinus imperator). 2, A subvertical tunnel produced by P. imperator. 3, A gold skink (Mabuya multifasciata). 4, A subvertical tunnel produced by M. multifasciata.5, A tiger salamander (Ambystoma tigrinum). 6, A subvertical tunnel produced by A. tigrinum.

 figure 9

FIGURE 10. Cluster analysis of burrows produced by Scaphiopus holbrookii and Pandinus imperator. Major clusters discussed in the text are denoted with the letter of the cluster in a yellow circle. The color of the burrow specimen number indicates the tracemaker: green = S. holbrookii; red = P. imperator. The similarity values of the clusters are marked with an arrow and a number.

figure 10 

FIGURE 11. Cluster analysis of burrows produced by Scaphiopus holbrookii and Mabuya multifasciata. The color of the burrow specimen number indicates the tracemaker: orange = M. multifasciata. For additional formatting descriptions refer to Figure 10.

figure 11 

FIGURE 12. Cluster analysis of burrows produced by Scaphiopus holbrookii and A mbystoma tigrinum. The color of the burrow specimen number indicates the tracemaker: purple = A. tigrinum. For additional formatting descriptions refer to Figure 10.

figure 12 

FIGURE 13. Cluster analysis of burrows produced by Scaphiopus holbrookii, Pandinus imperator, Mabuya multifasciata, and Ambystoma tigrinum. For formatting descriptions refer to the captions of Figure 10, Figure 11, and Figure 12.

figure 13 

FIGURE 14. Anomalous burrow architecture (SH16) defined as a resting trace. 1, View from the side. 2, View from the bottom of the burrow.

figure 14 

 

 

johnsonLauren M. Johnson. Department of Geological Sciences, Ohio University, 316 Clippinger Laboratories, Athens, Ohio 45701, USA This email address is being protected from spambots. You need JavaScript enabled to view it.

Lauren Johnson completed her Bachelor's Degrees in both Geological Sciences and Anthropology at Ohio University in 2015. She currently works for Big Brothers Big Sisters.

 

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hembreeDaniel I. Hembree. Department of Geological Sciences, Ohio University, 316 Clippinger Laboratories, Athens, Ohio 45701, USA This email address is being protected from spambots. You need JavaScript enabled to view it. Corresponding author

Daniel Hembree is an Associate Professor in the Department of Geological Sciences at Ohio University. His research interests primarily lie with animal-substrate interactions in ancient and modern continental environments. These interactions are preserved in the fossil record as trace fossils. Trace fossils provide an in situ record of ancient biodiversity, ecology, and environment. The study of trace fossils, therefore, provides vital information for accurate paleoenvironmental reconstructions. This involves not only the study of paleosols and continental trace fossils throughout geologic time, but also the experimental study of burrowing behaviors of extant terrestrial annelids, arthropods, amphibians, and reptiles. Current research projects involve the study of the influence of climate changes on ancient soils and soil ecosystems including those of the Pennsylvanian and Permian of southeast Ohio, Permian of eastern Kansas, and the Eocene to Miocene of Colorado and Wyoming.