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How does a change in labial tooth row number affect feeding kinematics and foraging performance of a ranid tadpole (Lithobates sphenocephalus)?

Introduction

Generalized pond-type anuran tadpoles forage either by passively filtering suspended food particles, such as phytoplankton and bacteria, from the water column (Gliwicz, 1969) or by sucking in a suspension of particles produced by actively grazing upon a substrate (Wassersug and Yamashita, 2001). The mechanism by which tadpoles passively filter and entrap food particles is particularly well studied (de Jongh, 1968; Kenny, 1969; Gradwell, 1972; Wassersug, 1972, 1973; Seale and Wassersug, 1979; Satel and Wassersug, 1981; Seale, 1982; Seale et al., 1982). In short, a pulse of water is brought into the tadpole's mouth by buccal pumping, and food particles suspended in the water are strained by papillae and gill filters or entrapped by mucus in the pharynx (Wassersug, 1973).

Less is known about how grazing tadpoles generate a particle suspension in the first place, although it is clear that the keratinized jaw sheaths and tranverse rows of labial teeth are involved in foraging (Johnston, 1982; Carr and Altig, 1991; Taylor and Altig, 1995; Taylor et al., 1996; Wassersug and Yamashita, 2001; Larson and Reilly, 2003). For example, Johnston (1982) showed that after grazing on algae, tadpoles left marks on the substrate, and suggested that labial teeth anchored the oral disc to the substrate while the tadpoles removed food from the substrate with their jaw sheaths. Wassersug and Yamashita (2001) used high-speed video to directly observe foraging kinematics of bullfrog (Lithobates catesbeianus [ =Rana catesbeiana] Shaw, 1802) tadpoles and demonstrated that in a single gape cycle (i.e., the opening and closing of the jaw sheaths and labial teeth), the labial teeth anchor the oral apparatus to the substrate (Wassersug and Yamashita, 2001), supporting Johnston's (1982) hypothesis on the function of the labial teeth. However, in addition to anchoring the oral disc, it was found that the labial teeth functioned in concert with the jaw closing to rake material off the substrate that is then sucked into the mouth of the tadpole during the next gape cycle (Arens, 1994; Wassersug and Yamashita, 2001).

In addition to the facultative role of the labial teeth in feeding, their shape and the number and size of tooth rows vary greatly among anuran species (Altig and McDiarmid, 1999). This ecomorphological diversity in the labial teeth of tadpoles that live in diverse habitats likely reflects adaptations to specific features of the biotic and abiotic environments. For example, many rows of labial teeth may be an advantage for taxa in lotic environments where more teeth can better anchor the larvae to the substrates and keep the tadpoles from being swept downstream. Alternatively, fewer labial tooth rows may be advantageous for taxa that live in lentic habitats where they do not face selection pressures to strongly adhere to a substrate.

Clearly, keratinized jaw sheaths and labial teeth play an important role in tadpole survival (i.e., food acquisition) and anuran evolution. Yet data relating foraging kinematics of tadpoles with variation in labial teeth number are rare (Venesky et al., unpubl. data; this study), despite increasing reports of the incidence of deformation to these structures. Deformations in labial teeth and jaw sheaths can occur naturally throughout ontogeny (Drake et al., 2007). However, a number of biotic and abiotic variables are associated with oral deformities. For example, portions of or entire keratinized structures are reported either missing or deformed in response to biotic stressors such as temperature (Bresler and Bragg, 1954), nutrition (Altig and McDiarmid, 1999), increased competition (Brett et al., 2009), high risk of predation (Relyea and Auld, 2005), pollution (Rowe et al., 1996, 1998), and pathogens (Drake et al., 2007). Given the contribution of pollutants and pathogens to the global decline of amphibian populations (Berger et al., 1998; Daszak et al., 2003) and their impact on tadpole mouthparts, data relating feeding kinematics of tadpoles with deformed or missing keratinized mouthparts are relevant in assessing the effect mouthpart abnormalities have on overall larval survival.

Thus, we explore here the impact of missing labial teeth on the feeding performance of tadpoles of the Southern leopard frog (Lithobates sphenocephalus [ = Rana sphenocephala] Cope, 1886). We experimentally controlled the pattern of labial tooth loss by surgically removing one row of labial teeth and compared the feeding kinematics, foraging behavior, and foraging efficiency of tadpoles with missing labial teeth to those of tadpoles with intact labial teeth. In our first experiment, we used high-speed (500 frames/second, hereafter "fps") videography of tadpoles to test the hypothesis that labial tooth loss reduces the amount of time that tadpoles attach to and graze upon a substrate covered with algae. We predicted that mouthparts of tadpoles from our surgery treatment would slip while foraging and that the duration of their gape cycle and the amount of time their labial tooth rows were in contact with the algal-covered substrate would be shorter than those of control tadpoles. In our second experiment, we used tadpoles similar to the ones in Experiment 1 and conducted trials of foraging efficiency and foraging activity to test the hypothesis that tadpoles with fewer labial teeth forage less effectively than control tadpoles. We predicted that tadpoles from the surgery treatment would obtain less food during a foraging trial compared to tadpoles from the control treatment. We also predicted that compared to tadpoles with intact mouthparts, tadpoles from our surgery treatment would spend more time in feeding activities to compensate for reduced foraging efficiency.

Materials and Methods

Animals

The 40 Southern leopard frog (Lithobates sphenocephalus) tadpoles used in these experiments were laboratoryborn progeny of five egg masses collected on 25 February 2009 in Shelby County, Tennessee (35[degrees]8'N, 89[degrees]4'W). Tadpoles were raised at 19-21 [degrees]C in the laboratory, where they were housed individually in 1.5-1 plastic containers with about 750 ml of aged tap water. They were kept on a natural light cycle and fed Sera Micron (Sera, Germany) daily. We changed the water weekly by siphoning about 70% of the water from the container and replacing it with the same volume of aged tap water. During our experiments, the tadpoles ranged in total length from 17.1 to 24.0 mm (20.9 [+ or -] 0.7; mean [+ or -] standard error) and in Gosner (1960) stage from 27 to 30.

Surgical removal of labial teeth

We randomly selected a subset of tadpoles (n = 16) from our stock for the surgery treatment in Experiments 1 and 2. Prior to surgery, we placed individual tadpoles in about 25 ml of MS222 (tricaine methanesulfonate), diluted to 0.06 g/1, until the tadpole was anesthetized and lost righting ability. We then transferred the tadpole to a wax dissection tray and positioned it ventral side up with enough MS222 solution to cover its body. With the tadpole under a dissecting scope, we used iridectomy scissors to remove the outermost posterior labial tooth row (P-3). Good exposure to the row was achieved by pressing lightly on the ventral side of the tadpole with a finger. The row was removed by a series of horizontal cuts at the base of the labial tooth row. During one surgery, a small portion of the lower papillae (about 1/10 of the length) was nicked, which caused a small amount of bleeding that clotted within seconds. All other surgeries were blood free.

After the removal of the labial tooth row, we returned each tadpole to its focal container and aerated the water for 30 min. Each tadpole was anesthetized for about 10 min and was able to swim about 10 min after the surgery. Tadpoles were given 3 days to recover from surgery before being used in the videography and foraging experiments, and all tadpoles foraged within a day of surgery.

Experiment 1: Foraging kinematics

To produce a standardized substrate on which the tadpoles could graze, we submerged microscope slides in a 4.5-1 plastic container with aged tap water and placed the container by a window for 2 weeks to allow epiphytic algae to colonize the microscope slides (following Wassersug and Yamashita, 2001). Before the start of a video trial, we scrubbed one side of an algal-covered slide to remove the algae and mounted the cleaned side of the slide against the inside wall of an acrylic plastic container (12.7 x 11.4 x 10.2 cm) where the tadpoles were videographed. The container was filled with about 750 ml of aged tap water, which was continually but gently aerated during each videography trial. For greatest resolution, we prefocused the camera on the inside surface of the microscope slide, which was covered with a dense layer of epiphytic algae. Different algal-covered slides were used for each videography trial, and slides appeared equally covered with algae. To encourage grazing, the tadpoles were not fed the day before filming.

Tadpoles (n = 16) were split into two experimental groups: control tadpoles (n = 8) with no mouthpart manipulations and surgery tadpoles (n = 8) with the outermost posterior labial tooth row (P-3) removed. We elected to use different tadpoles for the two treatment groups rather than recording the kinematics before and after the surgeries so that there were no developmental differences in the foraging kinematics between the two treatment groups. The order of the observations between treatment groups was randomly distributed over two consecutive trial dates (Hurlbert, 1984).

We filmed the tadpoles in individual trials while they grazed on an algal-covered slide, recording a single feeding bout for each tadpole. We defined a feeding bout as the point when the mouth of the tadpole first touched the algal-covered slide until the tadpole fully released from the slide and swam away. Each feeding bout consisted of a continuous rapid series of at least 5 gape cycles (7.1 [+ or -] 0.6; mean [+ or -] standard error), during which the tadpoles scraped food from the algal-covered slide. As per Wassersug and Yamashita (2001), we defined one gape cycle as (1) starting with the jaw sheaths fully closed and the anterior and posterior tooth rows in closest proximity; (2) proceeding to the point at which the mouth is fully open and the labial tooth rows reach maximum gape; and (3) ending with full closure of the jaw sheaths and anterior and posterior tooth rows in closest proximity to each other. All videography trials were completed within 2 days of the start of the experiment.

We quantified the kinematics of two aspects of foraging related to the ability of the tadpole to obtain food. We recorded the duration (in milliseconds) of the entire gape cycle and also the time that the outermost anterior and posterior labial tooth rows (A-1 and P-2/P-3, depending on surgery treatment) were attached to the algal-covered substrate. We chose to focus our data observations on the outermost labial tooth rows because they are the first tooth rows to contact the substrate when feeding and the last to release from it--and they play an important role in anchoring and raking food (Wassersug and Yamashita, 2001; Venesky et al., unpubl.). Because the feeding bout contained varying numbers of gape cycles, we considered the mean time for each kinematic measurement during the foraging bout as a datum in our analysis. We used univariate analysis of variance (ANOVA) to test for differences between treatment groups (surgery and control) in the duration of time for the entire gape cycle and also for the closing phase of the gape cycle. Our data met all assumptions of these statistical tests. Statistical analyses were performed in SPSS PASW ver. 17 (SPSS Inc.).

Experiment 2: Foraging efficiency and activity

We tested the hypothesis that missing labial teeth reduced foraging efficiency of L. sphenocephala (n = 24; n = 8 for control, n = 8 for surgery, and n = 8 for anesthetized) tadpoles by examining the quantity of food consumed during one 3-h trial. Additionally, during the foraging efficiency trials, we also observed the foraging activity of the same subjects to test whether the surgical procedures used to remove the labial tooth row altered their behavior. All tadpoles used in this experiment were different than the tadpoles used in Experiment 1; however, the surgical methods used were the same as described above. Additionally, we used a third treatment group in this experiment: tadpoles anesthetized with MS222 but without any surgery performed. This third treatment group allowed us to test whether the application of MS222 alone altered the foraging efficiency or foraging activity of tadpoles.

Prior to the start of the foraging efficiency trial, tadpoles were deprived of food for 2 days to reduce their intestinal content. In addition, we checked the focal containers periodically during the 2 days prior to the experiment and removed any fecal matter (a food source for tadpoles). This is an effective method for reducing the intestinal content of tadpoles (M. Venesky, unpubl.). At the start of the 3-h trial, we placed a microscope slide colonized with epiphytic algae (described above) vertically on the side of the test subject's container. At the end of the trial, each test subject was removed from the container, sacrificed, preserved in formalin, and stored in 70% EtOH. All tadpoles were dissected on the same date of the experiment to accurately quantify algal consumption during the trial.

To quantify the amount of algae ingested during the experimental trial, we dissected the intestine (excluding the foregut and colon) and straightened without stretching the entire intestine on a dissection pan. We measured the length of the intestine in millimeters (to the nearest 0.05 mm) with calipers. We also measured the diameter (mm) of the intestine in three locations--the midpoint and the anterior and posterior ends. We took the mean of the three diameter measurements and then estimated the total volume of the intestine. The epiphytic algae grown on the microscope slides is green and provides a sharp contrast to an empty intestine, allowing us to calculate the percentage of the intestine filled with food that was consumed during the 3-h trial.

To test for differences in the foraging activity of tadpoles, we observed the foraging activity of tadpoles during a 10-min portion of the foraging efficiency trial. Each 10-min activity trial was divided into 20-s intervals, and we recorded whether the test subject foraged at any point during an interval. The proportion of intervals during which the test subject foraged during the 10-min experimental trial was calculated as an estimate of foraging activity. Similar estimates of activity levels have been used in other tadpole behavior experiments (Parris et al., 2006; Han et al., 2008). Note that our goal in these trials was to estimate the overall foraging activity of tadpoles, not to identify specific foraging behaviors or duration of feeding bouts. We used univariate ANOVA to test for differences in the percentage of intestine with food between the three treatments. We also used ANOVA to test for differences in the amount of time spent foraging between the three treatments (surgery, control, and MS222). When appropriate, we used Scheffe's post-hoc analysis. Our data met all assumptions of this statistical test. Statistical analyses were performed in SPSS PASW (version 17).

Results

Experiment 1: Foraging kinematics

The surgical removal of a single labial tooth row had profound impacts on the feeding cycle in Lithobates sphenocephala tadpoles. As we predicted, tadpoles from the surgery treatment gripped the algal-covered substrate for a shorter amount of time (ANOVA; df = 14; F = 16.19; P < 0.0001; Fig. 1A, B) than tadpoles from the control treatment. Our high-speed video confirms that although the labial tooth rows of surgically treated tadpoles contacted the algal-covered substrate, they slid across the surface much faster than the tooth rows of control tadpoles (compare Figs. 2 and Fig. 3, and see Videos 1 and 2 at http://www.biobull.org/supplemental/). For example, from maximum gape to complete jaw closure in the control tadpole, the lower labial tooth rows maintained contact with the algal covered surface (Fig. 2, Video 1). The same sequences in the surgery tadpole (Fig. 3, Video 2) show the slipping of the remaining two labial tooth rows, causing the labial tooth rows to release in parallel, rather than sequentially. This resulted in a 34% decrease in the amount of time that the labial teeth of the tadpoles from the surgery treatment held the algal-covered substrate compared to control tadpoles.

Interestingly, the impact of the surgery was not restricted to only the closing of the jaws, but rather impacted the entire gape cycle. Tadpoles from the surgery treatment reached maximum gape in approximately 50% less time than tadpoles from the control treatment. This resulted in a shorter gape cycle for tadpoles from the surgery treatment (ANOVA; df = 14; F = 8.190; P < 0.0001; Fig. 1B) compared to tadpoles from the control treatment. Because of the shorter gape cycle, tadpoles from the surgery treatment completed about 25% more gape cycles per unit time compared to control tadpoles.

[FIGURE 1 OMITTED]

Experiment 2: Foraging efficiency and activity

Our data on foraging efficiency and activity demonstrate that anesthetized tadpoles are as active as control tadpoles and confirm that anesthetizing tadpoles did not solely contribute to any differences in foraging efficiency and feeding activity (P > 0.05). Contrary to our predictions, the difference in the gripping ability between tadpoles with or without a P-3 tooth row, as observed in Experiment 1, did not alter the amount of food ingested over the 3 h of foraging in Experiment 2 (ANOVA; df = 24; F = 0.107; P = 0.899; Fig. 4). Thus, although tadpoles with a surgically removed labial tooth row do not grasp an algal-covered substrate as long or as well as control tadpoles, they obtain equal amounts of food over a 3-h trial.

[FIGURE 2 OMITTED]

In our foraging behavior studies (Experiment 3), the data on the amount of time that tadpoles spent foraging are somewhat ambiguous. Univariate ANOVA revealed an overall significant effect of treatment on the percentage of time spent foraging (ANOVA; df = 24; F = 3.665; P = 0.043), with the tadpoles missing a tooth row spending the greatest amount of time searching for food. Yet Scheffe's post hoc analysis did not reveal any significant pairwise differences between the three treatments in time foraging. On average, tadpoles from the surgery treatment foraged 45% and 58% more than tadpoles from the control and anesthetized treatments, respectively. Although not statistically significant, our data from the foraging activity experiment are consistent with the kinematic data--tadpoles with surgically removed labial teeth forage more often than control tadpoles.

[FIGURE 3 OMITTED]

Discussion

The results from our experiments reveal the functional plasticity of keratinized mouthparts of anuran tadpoles and document the negative effects that missing labial teeth have on tadpole foraging performance. Removing a single row of labial teeth (P-3) in Lithobates sphenocephalus tadpoles alters their feeding kinematics, changes their foraging efficiency, and reveals some constraints missing teeth have on feeding. The remaining labial teeth in tadpoles that have had a single labial tooth row removed slip more while trying to grip the substrate than those of controls. Consequently, tadpoles from the surgery treatment exhibited a 34% decrease in the amount of time they were attached to an algal-covered substrate. Although we did not separately control for the anesthetic in our feeding kinematic experiment, all tadpoles appeared to recover from the MS222 within 3 h. Additionally, they were then given 3 days to further heal and acclimate to their surgery, during which their water was changed to ensure that there was no residual MS222 in the water. If the MS222 had a lingering effect on tadpoles from the surgery treatment, we would have expected to see that effect manifested in a slower gape cycle, whereas we observed the opposite. This result, plus the lack of an effect of MS222 on the feeding activity and feeding efficiency, suggests that the difference in feeding kinematics between treatment groups is from the missing teeth and not the anesthetic.

[FIGURE 4 OMITTED]

A second impact of labial tooth loss was that tadpoles from the surgery treatment increased the speed of their entire gape cycle. Compared to control tadpoles, tadpoles from the surgery treatment reached maximum gape about 50% faster and had about 25% more gape cycles per unit time. Although the kinematics of feeding differed between the treatment groups, tadpoles from control and surgery treatments obtained similar amounts of food during a 3-h foraging trial and actively foraged for similar amounts of time. Thus, while there was no negative effect of missing teeth on the net volume of food obtained at the end of the foraging trial, the efficiency at which tadpoles with missing labial teeth obtain food is likely compromised by spending more energy on foraging activities, most notably in increased numbers of gape cycles.

Our data show that tadpoles can compensate for missing labial teeth by increasing the speed of their gape cycles. Tadpoles have an elegant and complex set of muscles for closing their jaws. It is likely that different muscles are recruited when the jaws are closed at different speeds or challenged by substrates of different resistance (see, for example, the discussion in Larson and Reilly, 2003, on the levator mandibulae longus superficialis during the closing phase of the gape cycle. From a mechanical perspective, by increasing the speed at which they close their jaws, tadpoles generate more momentum and cutting force behind each gape cycle (Wassersug and Yamashita, 2001). Indeed, tadpoles increase the speed of their jaw movements when grazing on resistant surfaces (Wassersug and Yamashita, 2001). Tadpoles with missing labial teeth appear to be aware that the teeth are slipping and do not interpret that as efficient grazing on a substrate of low resistance. Tadpoles missing a row of labial teeth have compensatory kinematics to help maintain feeding efficiency through a series of gape cycles. Specifically, tadpoles with missing labial teeth appear to recognize that they are not obtaining much food per gape cycle and compensate by increasing the speed at which they open and close their jaws.

Given the significance of keratinized structures in the foraging process (Wassersug and Yamashita, 2001) and that foraging kinematics are altered when labial teeth are missing (Venesky et al., unpubl.; this study), we were surprised that in the short term tadpoles from the surgery and from the control treatment obtained similar amounts of food. Recent reports of tadpoles raised with environmental pollutants (Rowe et al., 1996; Hopkins et al., 2000) or exposed to pathogens (Fellers et al., 2001; Marantelli et al., 2004; Drake et al., 2007) have revealed a high incidence of deformations to their keratinized oral structures. Damage to these structures can thereby negatively impact feeding kinematics (Venesky et al., unpubl.; this study) and can possibly lead to slower rates of growth and developmental in amphibians. By spending more energetic resources in acquiring food, tadpoles may decrease their resources allocated to growth and metamorphose at a smaller body size compared to tadpoles with undamaged dentition. For larval amphibians that develop in temporary aquatic ecosystems, reaching a minimum size for metamorphosis increases the probability of successfully metamorphosing (Wilbur and Collins, 1973), and any reductions in growth and development can increase the chances of entrapment in a desiccating temporary pond (Keisecker and Skelly, 2001) and decrease the ability to escape gape-limited predators (Kurzava, 1998). We suggest that, although the net volume of food obtained in the short term was similar between control and surgery treatments, missing labial teeth alter foraging kinematics such that overall feeding efficiency of tadpoles with damaged mouthparts is reduced; that is, tadpoles with missing labial teeth have to forage more often than tadpoles with intact mouthparts.

We recognize that differences in the magnitude of mouthpart deformation may differentially impact feeding kinematics and also foraging performance. For example, Venesky et al. (unpubl.) found that tadpoles infected with the pathogenic fungus Batrachochytrium dendrobatidis, which attacks the keratinized mouthparts, obtain less food during foraging efficiency trials. In that experiment, infected tadpoles had few labial teeth and considerable damage to the jaw sheath (Venesky, pers. obs.), which are typical symptoms of heavily infected tadpoles (Fellers et al., 2001; Marantelli et al., 2004). Additionally, morphological diversity in labial tooth density, number, and disposition of rows may reflect adaptations to different foraging modes (Altig, 2006), and deformations to keratinized jaw structures may differ between species (Drake et al., 2007). For example, tadpoles with many labial teeth and many rows may respond to deformations and injury to their mouthparts differently than tadpoles with fewer labial teeth and rows. Accordingly, future studies could examine the feeding kinematics of tadpoles with pathogen-induced mouthpart damage or compare the foraging strategies of tadpoles with different foraging structures, modes, or both.

Although the present study was not comparative in design, we can identify some generalities in the foraging kinematics of tadpoles from other species within Lithobates. Not surprisingly, the keratinized jaw sheaths and labial teeth of L. sphenocephalus and L. catesbeianus tadpoles function similarly (Wassersug and Yamashita, 2001). The labial tooth rows anchor the oral disc into the substrate, holding the jaw sheaths against the surface and, upon release in each gape cycle, raking detachable epiphytic material off the surface. The detached material is then sucked into the tadpole's mouth during the subsequent gape cycle. As observed in L. catesbeianus tadpoles (Wassersug and Yamashita, 2001), L. sphenocephalus tadpoles also sequentially released their posterior labial tooth rows, starting with P-l and ending with P-3, with each row further removing material from the substrate. This is an elegant and efficient biomechanical system. Our research shows, however, that the removal of a single row of labial teeth can drastically alter the kinematics not just of the holding and raking functions of the labial teeth, but of the whole gape cycle.

Acknowledgments

We thank R. Altig for providing comments during the planning stages of this experiment. Collection permits from Tennessee were obtained prior to collecting the animals used in these experiments, and all experimental procedures were approved by the University of Memphis IACUC. This publication was developed, in part, under GRO Research Assistance Agreement No. MA-916980 awarded by the U.S. Environmental Protection Agency to M. Venesky. It has not been formally reviewed by the EPA. The views expressed in this document are solely those of the authors, and the EPA does not endorse any products or commercial services mentioned in this publication. R. Wassersug's participation was supported by the Natural Science and Engineering Research Council of Canada.

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Received 4 August 2009; accepted 13 December 2009.

* To whom correspondence should be addressed. E-mail: mvenesky@memphis.edu

MATTHEW D VENESKY (1), *, RICHARD J WASSERSUG (2), MATTHEW J PARRIS (1)

(1) Department of Biology, University of Memphis, Memphis, Tennessee 38152; and (2) Department of Anatomy and Neurobiology, Sir Charles Tupper Medical Building, Dalhousie University, Halifax, Nova Scotia B3H 4H7, Canada
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Author:Venesky, Matthew D.; Wassersug, Richard J.; Parris, Matthew J.
Publication:The Biological Bulletin
Article Type:Report
Geographic Code:1CANA
Date:Apr 1, 2010
Words:5336
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