Mother-offspring chemical communication and tadpole aggregation in a Neotropical foam-nesting frog

doi:10.21203/rs.3.rs-3304603/v1

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Mother-offspring chemical communication and tadpole aggregation in a Neotropical foam-nesting frog

https://doi.org/10.21203/rs.3.rs-3304603/v1

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published 23 Apr, 2024

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Communication during parental care represents an advantage for eliciting offspring behaviour and sibling recognition. In aquatic environments, chemical communication is usually the most effective, playing different roles in amphibian parental behaviour. Attending females of some Neotropical anurans (Leptodactylus) lead entire tadpole schools through the water. However, little is known about this aggregation behaviour, such as the type of signal used by attending females or if they are specific between mothers and offspring. Here we conducted behavioural experiments to investigate these questions. Firstly, we tested the effect of visual, tactile, and chemical stimulus of attending females on tadpole aggregation behaviour. Following, we compared the effects of the chemical stimulus from attending females with those from other conspecifics (non-attending females and males) on schooling behaviour. Finally, we tested whether tadpoles prefer related attending females instead of unrelated ones. Our results indicated that only chemical stimulus from attending females, and not visual or tactile, increased tadpoles´ aggregation time. Chemical stimulus from non-attending females and males did not affect tadpoles’ behaviour. Contrary to what we expected, we did not find school preference for related attending females. We were able to demonstrate the presence of chemical signals in mother-tadpole school relationship of Leptodactylus species. Besides, we showed that chemical signals both attract and aggregate tadpoles, which can be crucial for attending females, who guide the entire school through aquatic habitats. Furthermore, our results suggest that tadpoles do not prefer related attending females and may benefit from following unrelated attending female tacking advantage of alloparental care.

Parental care

Parent-offspring interaction

tadpole schooling

kin recognition

maternal care

Parental care represents an advantage for offspring survival and parents-offspring communication may be helpful. In aquatic environments the role of chemical signals presents several advantages, reason why, we study the effects of attending females’ chemical signals over free swimming tadpoles’ behaviour. We found that the chemical signal of attending females favours tadpoles’ aggregation and it has an attraction effect, helping attending females to protect tadpoles. Additionally, we demonstrate that tadpoles use the protection of any attending females rather than prefer blood related attending females, which may favour tadpoles’ survival while it may increases attending females cost.

Communication is defined as the transmission of information from a sender to a receiver, leading to changes in receiver behaviour (Kaplan 2014). Animal communication can be intraspecific or interspecific, and plays many important functions, such as territorial defence, rival warning, courtship behaviour, prey location, and parent-offspring interaction (Bradbury and Vehrencamp 2011; Wyatt 2014). The information flows through diverse stimuli such as signals or cues, and signals (unlike cues) are evolutionarily selected due to the effect they have on the receiver, generally leading to changes in behaviour (Bro-Jørgensen 2010; Schulte et al. 2015; Brunetti et al. 2018). Main signals used in animal communication include visual, acoustic, chemical, and tactile (Mattey et al. 2018).

Chemical signals are the most ancient and widespread form of animal communication, mostly used during courtship (Johansson and Jones 2007; Meinwald and Eisner 2008; Wyatt 2014). However, they also play a fundamental role in parental care by mediating begging behaviour in insects and anurans offspring (Kam and Hang 2002; Smiseth et al. 2010), feeding in birds and mammals (Schaal et al. 2003; Balthazart and Taziaux 2008), or mutual parent-offspring recognition in beetles and mammals (Smiseth et al. 2010; Schaal et al. 2003). In aquatic environments, chemical signalling has several advantages because transmission of acoustic and visual signals may be hampered and less effective (Brönmark and Hansson 2000; Rosnthal and Ryan 2000). One relevant function of chemical communication in aquatic environments is to be used by parents to guide and maintain cohesion of offspring, as observed in non gregarious cichlids and suggested for anurans with schooling behaviour (Myrberg 1975; Barnett 1977; Wells and Bar 1988).

Aggregation is a common social behaviour among aquatic organisms, where they come together and perform coordinated movements with adaptive functions (Pavlov and Kasumyan 2000). This behaviour is well known in fish and tadpoles and is an effective antipredator strategy that confuses predators and dilutes the risk of predation (Hobson 1978; Caldwell 1989; Lehtonen and Jaatinen 2016). Tadpoles from 12 anuran families are known to exhibit aggregation behaviour (Wells 2007). In Neotropical leptodactylid frogs, aggregation behaviour depends on external social stimuli (Ponssa 2001) and is usually accompanied by parental care (e.g. wells and Bard 1988; Martins et al. 2001). For instance, within species of the Leptodactylus melanonotus and L. latrans groups, females attend to eggs and guide aquatic tadpoles, dig channels to connect water bodies, and protect them from predators by performing aggressive behaviours (Wells and Bard 1988; Prado et al. 2000; Martins 2001; Rodrigues et al. 2011; Castro et al. 2013; Sestito et al. 2016; Carrillo et al. 2023).

In these Leptodactylus species with maternal care, tadpole orientation and guidance are mediated by the "pumping" behaviour (sensu Wells and Bard 1988) performed by the female. The attending female hits the water surface with her pelvis to generate waves and the tadpole school follows and scrape the female´s back (Wells and Bard 1988; Martins 2001; Wells 2007; Castro et al. 2013; Carrillo et al. 2022). Pumping behaviour is suggested to be mediated by a tactile stimulation, but it may be other factors such as chemical stimulus that attract, orient, aggregate, and guide tadpoles through obstacles to deeper aquatic sites (Wells and Bard 1988; Vaira 1997; Hoffmann 2008). The communication between attending females and tadpole schools may involve three different stimuli: visual, tactile, and chemical. However, this prediction has never been experimentally tested, and parent-offspring communication in anurans remains poorly understood.

Taking all of this into consideration, we aim to better understand mother-offspring communication and kin recognition in a neotropical foam nesting frog (Leptodactylus podicipinus). Therefore, with three independent experiments, we addressed the following questions: 1) Which type of stimulus (visual, tactile and/or chemical) mediates tadpoles´ aggregation behaviour? 2) Are these chemical stimuli produced only by attending females, or also by other conspecifics (non-attending females, males)? 3) Do tadpoles prefer to aggregate next to related attending females over unrelated ones? Based on previous studies, field observations and considering the implications of chemical communication underwater, we hypothesize that chemical stimulus is the most effective in promoting aggregation of tadpoles. Furthermore, we expect that tadpoles will be capable of discriminating between the chemical stimulus of attending female and those from other conspecific adults (non-attending females and males), aggregating more next to attending females. Finally, if tadpoles are able to discriminate chemical stimulus of related attending females from those emitted by unrelated attending females, they will prefer to aggregate next to related attending females, due to genetic relationship.

During the rainy seasons of 2019 and 2021 (November to March), we collected attending females with their tadpole schools at the Estância Crioula ranch (20°32'13.51"S, 55°32'53.69"W). Estância Criola is located in the Cerrado, the most diverse tropical savanna and one of the main hotspots for global conservation due to its high biodiversity and pressing threats (Eiten 1994; Myers et al. 2000; Alvares et al. 2013).

in Cerrado the reproductive activity of Leptodactylus podicipinus (Fig. 1) is restricted to the rainy season from November to January (JFC Carrillo pers. obs.), females attend large schools till the end of the metamorphosis (Martins 2001). We captured a total of 14 schools of L. podicipinus with their attending females. Leptodactylus podicipinus schools contained from 112 to 701 tadpoles (x = 404 ± 173, N = 14). Following Gosner (1960) stages of development, 50% of the schools had tadpoles from one stage of development, 29% from two different stages, and 21% from three different stages (Supplementary 1). We captured the animals under SISBIO Brazilian License (68071-4), with bioethical approval of CEUA/UFMS (1.085/2019), and we stored adults and tadpoles in the zoological collection of the Universidade Federal de Mato Grosso do Sul (ZUFMS-AMP − 14661–14668, 14670–14698, 14710–14723).

Experiment 1 was designed to investigate the type of stimulus (visual, tactile, or chemical) used by attending females to promote tadpole aggregation, in a smalls scale, using only 5 tadpoles per replica. Once we identified the effects of chemical stimulus on tadpole aggregation (see Results), the experiment 2 to test if tadpoles respond only to stimulus produced by attending females, or by other conspecifics as well, by using the entire schools and the adults as stimulus source. Additionally, we made behavioural observations to describe school behaviour. The experiment 3 intended to assess if tadpoles prefer to aggregate next to related attending females over unrelated attending females.

Experiment 1: Attending female stimuli

After capture, we transported the organisms to the Laboratory of Ecology of the Universidade Federal de Mato Grosso do Sul (UFMS, Campo Grande, MS, Brazil). Animals were transported in coolers with compartments containing water from the sample site separating schools and attending females. Later, we placed each school in separate aquariums (40x20x30 cm) without the attending female for one day of acclimation at environmental temperature (27–29°C) and a 12 to 12 h photoperiod.

The next day, we conducted three trials of each treatment (visual, tactile, or chemical stimulus) and their respective controls, with 12 replicas per trial. To test for tadpole aggregation in response to visual stimulus, we used a plastic frog doll to simulate attending female presence (visual stimulus) and a plastic ball as control. To test for tadpole aggregation in response to tactile stimulus (attending female pumping behaviour generating waves), we simulated the waves manually with a hanging cylinder (5 mm radium and 60 mm long), and we used the same cylinder, this time without movement, as control. To test for tadpole aggregation in response to chemical stimulus, we extracted and collected attending female skin secretion with a cotton ball using a mild electric stimulation (see Tyler et al. 1992) and we used a fresh sterile cotton ball as control. For each experiment, we placed five L. podicipinus tadpoles from the same school in Petri dishes (30 mm of diameter) filled with fresh rainwater, guaranteeing enough vertical space to swim. After three minutes of acclimation in the Petri dish, we placed the respective stimulus fixed to the border. For each replica, we used different tadpoles. For more details of the experiments see Supplementary 2.

Tadpoles’ behaviour was video recorded for seven minutes. We used Behavioural Observation Research Interactive Software BORIS (Friard and Gamba 2016) to register the aggregation time (accumulative time of tadpoles aggregation). For the purpose of this experiment, we defined aggregation time as the time that three or more tadpoles remained close together (see Pavlov and Kasumyan 2000). For each trial (visual, tactile, and chemical signal experiments), we fitted a linear mixed effect model in R 4.0.4. (R Core Team, 2021), with aggregation time as response variable, treatment (stimulus vs control) as fixed factor and school as random intercept, using the nlme package (Pinheiro et al. 2021).

Experiment 2: Intraspecific chemical stimuli

After field collection, the entire school of Leptodactylus podicipinus was placed in a tray (350 x 240 mm) and filled with pond water collected with the tadpoles. Stimulus was placed in one of four quadrant corners. For every trial replicate, totalling 28, we changed stimulus corner position randomly and we waited at least 10 minutes between replicates to allow water homogenization. Stimulus consisted in a cup with holes with one of three conspecific adults: attending female, non-attending female or male. As control we used a cup without holes with an attending female (Supplementary 3). Tadpoles’ behaviour was video recorded for seven minutes. We made behavioural observations to describe schooling features and we registered aggregation time (seconds) using BORIS software (Friard and Gamba 2016). In addition to aggregation time, we added an additional response variable to test if the attending females were able to attract tadpoles. For that we measured the aggregation time next to the stimulus (seconds). Aggregation was defined as the time when more than 90 percent of the school of tadpoles grouped (see Pavlov and Kasumyan 2000). Aggregation time next to the stimulus was the time tadpoles were grouped within the corner where the cup with the adult was placed (supplementary 3). Since data from this experiment did not meet criteria for parametric statistics, it was analysed by Kruskal-Wallis and post-hoc Dunn tests in R 4.0.4 (R Core Team 2021).

Experiment 3: School preference for related/unrelated attending female

Experiment 3 follows guidelines and analyses from experiment 2. After placing the school in the middle of the trail, we simultaneously placed a related and a unrelated attending females in opposite corners of the tray (350x240 mm), to measured aggregation time next to unrelated attending females, next to related attending females and far from both (Supplementary 4). This process was repeated in six replicas with different tadpoles. Besides the Kruskal-Wallis test for accumulative aggregation time, we analysed how frequently tadpole schools first aggregated next to related over unrelated attending females by a Chi-Square test in R 4.0.4 (R Core Team 2021).

Experiment 1: Attending female stimuli

Descriptive data of the three types of signals from attending females and controls tested are presented in Table 1. Aggregation time of tadpoles of L. podicipinus only differed significantly in the chemical stimulus treatment, increasing from aggregation time of 28.97 ± 19.13 s in the control to an aggregation time of 113.98 ± 39.15 s (t = 4.77, p < 0.001, N = 12; Fig. 2) in the chemical signal treatment. Aggregation time of tadpoles did not vary significantly under visual and tactile signals when compared with their respective controls (t = 1.47, p = 0.17, N = 12; t= -1.74, p = 0.11, N = 12; respectively) (Fig. 2).

Table 1

Aggregation time (seconds) of the tadpoles of *Leptodactylus podicipinus* under three attending female stimuli (Experiment 1).
	Control				Stimuli
	Mean	SD	Max	Min	Mean	SD	Max	Min
Chemical	28.97	19.13	59.35	2.57	113.98	39.15	154.23	40.11
Tactil	36.63	8.45	51.63	26.31	30.20	3.10	35.59	27.11
Visual	44.51	20.66	79.63	21.10	74.10	44.61	126.00	7.10

Experiment 2: Intraspecific chemical stimuli

Tadpole schools of L. podicipinus presented two types of aggregation behaviours: constant movement aggregation and stationary aggregation (Supplementary 5). In constant movement aggregation, tadpoles moved all together in a cohesive way with limited space between them, following the tray edges. In stationary aggregation, tadpoles stayed at the bottom of the water, close to the stimulus, with space between them, and moving only to recover the lost position after water movement.

Measures of aggregation time and aggregation time next to the stimulus (male, non-attending female, attending female) for tadpole schools of L. podicipinus are presented in Table 2. We did not find differences between the aggregation time (Kw-chi = 2.71, p = 0.43, N = 25). However, aggregation next to the stimulus showed significant differences (Kw-chi = 18.53, p < 0.001, N = 25). Specifically, aggregation time next to the stimulus was significantly higher for attending females when compared with the control, males, and non-attending females (Dunn = 3.16, p < 0.001; Dunn = 3.97, p < 0.001; Dunn = 3.21, p < 0.001) (Fig. 3).

Table 2

Aggregation time (seconds) and aggregation time next to the tadpoles of *Leptodactylus podicipinus* under three conspecific chemical stimuli (Experiment 2).
	Aggregation				Aggregation At the Stimulus
	Mean	SD	Max	Min	Mean	SD	Max	Min
Control	29.09	28.62	74.71	0.24	3.94	7.29	18.63	0.00
Male	24.76	23.49	62.99	6.50	0.00	0.00	0.00	0.00
No-Attending Female	10.12	11.05	28.84	0.00	1.20	2.68	6.00	0.00
Attending Female	89.9	86.55	222.11	0.00	244.84	108.94	366.00	107.88

Experiment 3: School preference for related/unrelated attending female

Tadpoles spent more time aggregated next to the related attending female (230.01 ± 179.77 s) than next to unrelated attending female (117.70 ± 182.35 s) or far from the females (14.64 ± 20.72 s). However, the difference was not significant (Kw-chi = 0.82, p = 0.97, N = 18; Fig. 4). Regarding school preference, we found no differences in tadpoles choosing to aggregate next to related or unrelated attending females (chi = 1.33, p = 0.24, N = 12).

Given that attending females pumping behaviour denotes a voluntary nature (sender), and considering the effects of chemical stimulus over tadpoles (receiver) behaviour, we can assume that tadpoles’ aggregation and attraction to attending females is the result of a chemical signal (see Schulte et al. 2015). We experimentally demonstrated the importance of chemical signal for mother-tadpole communication in Leptodactylus podicipinus, resulting in tadpole aggregation and attraction to attending female. Tadpoles responded by actively aggregating themselves and following the chemical signal of the attending female, while visual or tactile signals had no effect. In a previous study with L. insularum (referred as bolivianus), Wells & Bard (1988) pointed out that tadpole aggregation and attraction could involve not only tactile stimulus (waves) produced by attending females, but also chemical signal. Accordingly, Hoffmann (2006) predicted a “beneficial or attractant” mucus secretion by the attending females secreted to keep school cohesion, and subsequently lead the tadpoles. Although our results did not show tactile effect on schooling behaviour, we demonstrated that tadpoles respond to chemical secretions produced by attending females increasing the time of aggregation.

The main purpose of aggregation is to reduce the risk of predation (Manna et al. 2018). In fish, chemoreception plays a crucial role in aggregation and orientation, but only under particular circumstances (Hara 1975). At night (under low visibility), fishes aggregate using intraspecific chemical cues (Keenleyside 1955; Jones 1962), and at the daytime, under the presence of predators, they can aggregate by using alarm cues (Rüppel and Gosswein 1972). In anuran larvae, aggregation depends on social factors such as tadpole density, predator presence or warning cues (Ponssa 2001; Spieler and Linsenmair 2001). Although visual signals may help to improve assembling the school (Blaustein and O’Hara 1982), in all scenarios, aggregation may be the result of chemical communication, triggered by a chemical signal/cue produced by siblings (Blaustein and O’Hara 1982). Here we found a similar trigger for tadpole aggregation in a species with parental care, where the chemical signal comes from the attending female.

Contrary to our expectations, experiments did not find any preference of schools for related over unrelated attending females. Tadpoles seem to follow equally the chemical signal of related and unrelated attending females, suggestion no kin recognition by tadpoles in relation to attending females. We hypothesize that tadpoles may benefit equally by receiving care and protection, and consequently, increasing their chances of survival whether the attending female is genetic related or not. This behaviour may lead to alloparental care, and it may be the reason why it is common to find schools with tadpoles in different stages of development (see supplementary 1). Additionally, field observations of two or even three schools of L. podicipinus mixing was common, which eventually broke up into small schools to follow attending females performing pumping behaviour (FC Carrillo, unpublished data). Interspecific schools of L. podicipinus and L. luctator, remaining grouped for more than 30 hours, with attending females performing pumping behaviour and guarding the tadpoles (Rodrigues et al., 2011).

Communication is fundamental for parental care and sibling recognition (Blaustein & O'Hara, 1982; Kam & Yang, 2002). For instance, cichlids can recognize related free-swimming offspring (Myrberg, 1975), and parents of blind goby fish avoid eating related offspring because they recognize them chemically (MacGinitie, 1939). In, species that provide food to their offspring use communication to know how much and when to provide it (Davis et al., 2019). This is the case of anurans that breed in phytotelmata, which use the water retained in plant axils for egg laying and tadpole development. As the water is poor in nutrients, tadpoles scrape attending female’s back (begging behaviour) to stimulate trophic eggs release (Summers & Tumulty, 2014) and attending females recognize offspring from unrelated tadpoles, as is the case of Oophaga pumilio (Stynosk, 2009) and Kurixalus eiffingeri (Kam & Hang, 2002). Although parents should be able to identify offspring to avoid alloparental care and parental fitness reduction (Trivers, 1972), offspring recognition by attending females of Leptodactylus seems unlikely because of the great number of tadpoles (see supplementary 1). Thus, in free swimming tadpoles, as in species of Leptodactylus, the main function of parental care is to protect tadpoles against predators and to keep them far away from deep waters, where predators are more abundant and food sources are limited (Vaz-Ferreira, 1975; Martins, 2001; Hurme, 2015; Carrillo et al., 2023). Tadpoles and females travel long distances (see Wells & Bar, 1988), and schools can follow attending females even through excavated channels and tunnels (Rodrigues et al., 2011; Hoffmann, 2006). Thus, we experimentally confirm, for L. podicipinus, that chemical signals play an important role in these complex behaviours. Moreover, we identified that chemical signals are specifically produced by attending females, not by non-attending females or males, proving to be proper chemical signals.

The chemical composition of amphibian skin has been primarily studied for their defensive properties, aiming to obtain bioactive substances, as reported in many reviews (e.g. Nascimento et al. 2003; Conlon et al. 2011; Thomas et al. 2012; Conlon et al. 2014; Xu and Lai 2015; Pantic et al. 2017; Rodriguez et al. 2017; Rodriguez et al. 2020). In amphibian social contexts, chemical compounds acting as pheromones during courtship and territorial disputes are some of the known functions (King et al. 2005; Starnberger et al. 2013). However, little is known about the substances involved in chemical communication during parent-offspring interaction, and future studies on Leptodactylus should focus on the identification of these compounds. This should combine chemical analyses and bioassays in order to understand the context and triggers of aggregation, and if aggregation is triggered by one or more chemical signals (see Schulte et al., 2015).

In conclusion, we showed that chemical signals are fundamental for mother-tadpole communication in the frog Leptodactylus podicipinus, playing an important role prompting aggregation (schooling behaviour) and attraction. Furthermore, our results indicate that school attraction does not seem to be mother-specific, therefore, tadpoles can follow unrelated attending females probably benefiting from alloparental care. Nonetheless, because females of many species of Leptodactylus perform “pumping” behaviour (sensu Wells & Bard, 1988), and diverse communication mode are known (Carrillo et al., 2023), further experiments are needed to investigate different signals that might be involved in the communication between attending females and offspring in the genus.

Acknowledgments

We thank Vanessa Stavis from Estância Crioula for all the logistic support. To Sabogal A and Oliveira-Santos LGR for help with data analyses. Carrillo JFC thanks the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior - Brasil (CAPES) - Funding code 001, for PhD fellowship. Santana DJ thanks the CNPq (Conselho Nacional de Desenvolvimento Científico e Tecnológico) for the research fellowship (309420/2020-2) and the Fundect for fellowship support (59/300.092/2017). Ortega Z thanks the Andalusian government (Spain) and FEDER EU funds for a Postdoctoral Research Contract (ref. 401).

Funding

This research was funded by the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior CAPES (ref. 001), the Conselho Nacional de Desenvolvimento Científico e Tecnológico CNPq (309420/2020-2), the Fundação de Apoio a Pesquisa ao Ensino e a Cultura FUNDECT (59/300.092/2017) and FEDER EU funds (ref. 401).

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

We captured the animals under SISBIO Brazilian License (68071-4). We conducted the experiments under bioethical approval of CEUA/UFMS from Universidade Federal de Mato Grosso do Sul, Brazil (ref. 1.085/2019).

Consent to participate

Not applicable

Consent for publication

Not applicable

Data availability

All data generated or analyzed during this study are included in this published article.

Code availability

Not applicable

Contributions

Carrillo JFC, Santana DJ and Prado CPA conceived and designed this study. Carrillo JFC conducted all experiments and analysed the data. Carrillo JFC, Ortega Z, Santana DJ and Prado CPA wrote this manuscript. All authors substantially edited and approved the final manuscript.

Alvares CA, Stape JL, Sentelhas PC, Goncalves, JLD, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorol Zeitschrift 22(6): 711-728. https://doi.org/10.1127/0941-2948/2013/0507
Balthazart J, Taziaux M (2008) The underestimated role of olfaction in avian reproduction?. Behav Brain Res 200: 248-259. https://doi.org/10.1016/j.bbr.2008.08.036
Barnett C (1977) Chemical recognition of the mother by the young of the cichlid fish Cichlosoma citrimellum. Journal of Chem Ecol 3: 461-466. https://doi.org/10.1007/BF00988188
Blaustein AR, O’hara RK (1982) Kin recognition in Rana cascadae tadpoles: maternal and paternal effects. Anim Behav 30(4): 1151-1157. https://doi.org/10.1016/s0003-3472(82)80205-4
Bradbury JW, Vehrencamp SL (2011) Principles of Animal Communication. 2nd edn. Sinauer, Sunderland
Brunetti AE, Neto FC, Vera MC, Taboada C, Pavarini DP, Bauermeister A, Lopes NP (2018) An integrative omics perspective for the analysis of chemical signals in ecological interactions. Chem Soc Rev 47(5): 1574-1591. https://doi.org/10.1039/c7cs00368d
Brönmark C, Hansson LA (2000) Chemical communication in aquatic systems: an introduction. Oikos 88(1): 103-109. https://www.jstor.org/stable/3546400
Bro-Jørgensen J (2010) Dynamics of multiple signalling systems: animal communication in a world in flux. Trends Ecol Evol 25(5): 292-300. https://doi.org/10.1016/j.tree.2009.11.003
Caldwell JP (1989) Structure and behavior of Hyla geographica tadpole schools, with comments on classification of group behavior in tadpoles. Copeia 4: 938-948. https://doi.org/10.2307/1445980
Carrillo JFC, Santana DJ, Prado CPA (2023) An overview of parental care in the foam-nesting frogs of the genus Leptodactylus (Anura: Leptodactylidae): current knowledge and future directions. Amphib-Reptil 44(3): 301-311. https://doi.org/10.1163/15685381-bja10140
Castro DP, Borges-Leite MJB, Lima DC, Borges-Nojosa DM (2013) Parental care in two species of Leptodactylus Fitzinger, 1826 (Anura, Leptodactylidae) in north-eastern Brazil. Herpetol Notes 6: 267-269
Conlon JM (2011) Structural diversity and species distribution of host-defense peptides in frog skin secretions. Cell Mol Life Sci 68: 2303-2315. https://doi.org/10.1007/s00018-011-0720-8
Conlon JM, Mechkarskaa M, Lukicc ML, Flatt PR (2014) Potential therapeutic applications of multifunctional host-defense peptides from frog skin as anti-cancer, anti-viral, immunomodulatory, and anti-diabetic agents. Peptide 57: 67-77. https://doi.org/10.1016/j.peptides.2014.04.019
Davis KL, Karpanty SM, Spendelow JA, Cohen JB, Althouse MA, Parsons KC, Luttazi CF (2019) Begging behavior as an honest signal of need and parent–offspring association during the post fledging dependency period. Ecol Evol 9(13): 7497-7508. https://doi.org/10.1002/ece3.5279
Dixon JR, Staton MA (1976) Some aspects of the biology of Leptodactylus macrosternum Miranda-Ribeiro (Anura: Leptodactylidae) of the Venezuelan llanos. Herpetol 32(2): 227-232. https://www.jstor.org/stable/3891743
Eiten G (1994) Vegetação do Cerrado. In: Pinto MN (Ed) Cerrado: Caracterização, Ocupação e Perspectivas. Editora da Universidade de Brasília, Brasília, pp 17-73
Friard O, Gamba M (2016) BORIS: a free, versatile open-source event-logging software for video/audio coding and live observations. Methods Ecol Evol 7(11): 1325-1330. https://doi.org/10.1111/2041-210x.12584
Glennemeier KA, Denver RJ (2002) Role for corticoids in mediating the response of Rana pipiens tadpoles to intraspecific competition. J Exp Zool 292: 32-40. https://doi.org/10.1002/jez.1140
Gosner KL (1960) A simplified table for staging anuran embryos and larvae with notes on identification. Herpetol 16: 183-190. https://www.jstor.org/stable/3890061
Hara TJ (1975) Olfaction in fish. Prog Neurobiol 5(4): 271-335
Hobson ES (1978) Aggregating as a defense against predators in aquatic and terrestrial environments. In E. S. Reese ES, Lighter FJ (Eds) Contrasts in behavior: adaptations in the aquatic and terrestrial environments. Wiley, New York, pp 219-234
Hoffmann, H. (2006). Observations on behaviour and parental care of Leptodactylus melanonotus (Hallowell) in Costa Rica. Salamandra 42(2/3): 109-116
Hurme KJ (2015) Reproductive and spatial ecology of Leptodactylus insularum (Anura, Leptodactylidae) in Panama. J Herpetol 49(1): 36-45. https://doi.org/10.1670/13-214
Johansson BG, Jones TM (2007) The role of chemical communication in mate choice. Biol Rev 82(2): 265-289. https://doi.org/10.1111/j.1469-185x.2007.00009.x
Jones FRH (1962) Further observations on the movements of herring (Clupea harengus L.) schools in relation to the tidal current. Journal du Conseil International pour l´Exploration de la Mer 27: 52-76. https://academic.oup.com/icesjms/article/27/1/52/581509
Kam YC, Yang HW (2002) Female–offspring communication in a Taiwanese tree frog, Chirixalus eiffingeri (Anura: Rhacophoridae). Anim Behav 64(6): 881-886. https://doi.org/10.1006/anbe.2002.2004
Kaplan G (2014) Animal communication. WIREs Cogn Sci 5(5): 661-677. https://doi.org/10.1002/wcs.1321
Keenleyside MHA (1955) Some aspects of the schooling behaviour of fish. Behaviour 8: 183-248. https://www.jstor.org/stable/4532829
King JD, Rollins-Smith, LA, Nielsen PF, John A, Conlon JM (2005) Characterization of a peptide from skin secretions of male specimens of the frog, Leptodactylus fallax that stimulates aggression in male frogs. Peptide 26: 597-601. https://doi.org/10.1016/j.peptides.2004.11.004
Kinosita H (1972) Schooling behaviour in marine catfish eel, Plotosus anguillaris. Zool Mag Kiel 81: 241.
Lehtonen J, Jaatinen K (2016) Safety in numbers: the dilution effect and other drivers of group life in the face of danger. Behav Ecol Sociobiol 70: 449-458. https://doi.org/10.1007/s00265-016-2075-5
MacGinitie GE (1939) The natural history of the blind goby Tvphlogobius californiensis (Steindachlner). Am Mid Nat 21: 489-505
Manna D, Maiti A, Samanta GP (2018) Analysis of a predator-prey model for exploited fish populations with schooling behavior. Appl Math Comput 317: 35-48. https://doi.org/10.1016/j.amc.2017.08.052
Mattey SN, Richardson J, Ratz T, Smiseth PT (2018) Effects of offspring and parental inbreeding on parent-offspring communication. Am Nat 191(6): 716-725. https://doi.org/10.1086/697236
Martins IA (2001) Parental care behavior in Leptodactylus podicipinus (Cope, 1862) (Anura, Leptodactylidae). Herpetol J 11: 29-32
Meinwald J, Eisner T (2008) Chemical ecology in retrospect and prospect. PNAS 105: 4539-4540. https://10.1073/pnas.0800649105
Myers N, Mittermeier RA, Mittermeier CG, Fonseca GAB, Kent J (2000) Biodiversity hotspots for conservation priorities. Nature 403: 853-858. https://doi.org/10.1038/35002501
Myrberg AA (1975) The role of chemical and visual stimuli in the preferential discrimination of young by the cichlid fish Cichlasoma nigrofaciatus (Giuather). Z Tierpsychol 37: 274-297. https://doi.org/10.1111/j.1439-0310.1975.tb00881.x
Nascimento AC, Fontes W, Sebben A, Castro MS (2003) Antimicrobial peptides from anurans skin secretions. Protein Pep Lett 10(3): 227-238. https://doi.org/10.2174/0929866033478933
Pantic J M, Jovanovic IP, Radosavljevic GD, Arsenijevic NN, Conlon JM, Lukic ML (2017) The potential of frog skin-derived peptides for development into therapeutically-valuable immunomodulatory agents. Mol 22(2071): 1-12. Https://doi.org/10.3390/molecules22122071
Pavlov D, Kasumyan AO (2000) Patterns and mechanisms of schooling behavior in fish: A review. J Ichthyol 40(2): S163-S23
Pinheiro J, Bates D, DebRoy S, Sarkar D (2021) nlme: Linear and Nonlinear Mixed Effects Models. R package version 3.1-152. https://CRAN.R-project.org/package=nlme
Ponssa ML (2001) Cuidado parental y comportamiento de cardumen en de larvas en Leptodactylus insularum (Anura, Leptodactylidae). Alytes 19(2-4): 183-195.
Prado CPA, Uetanabaro M, Haddad CFB (2005) Breeding activity patterns, reproductive modes, and habitat use by anurans (Amphibia) in a seasonal environment in the Pantanal, Brazil. Amphib-Reptil 26(2): 211-221. http://dx.doi.org/10.1163/1568538054253375
Prado CPA, Uetanabaro M, Lopes FS (2000) Reproductive Strategies of Leptodactylus chaquensis and L. podicipinus in the Pantanal. J Herpetol 34: 135-139. https://doi.org/10.2307/1565249
R Core Team (2021) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-roject.org/
Rodrigues AP, Giaretta AA, da Silva DR, Facure KG (2011) Reproductive features of three maternal-caring species of Leptodactylus (Anura: Leptodactylidae) with a report on alloparental care in frogs. J Nat Hist 45: 33-34. https://doi.org/10.1080/00222933.2011.574799
Rodriguez C, Ibáñez R, Rollins-Smith LA, Gutiérrez M, Durant-Archibold AA (2020) Antimicrobial Secretions of Toads (Anura, Bufonidae): Bioactive Extracts and Isolated Compounds against Human Pathogens. Antibiotics 9: 843. https://doi.org/10.3390/antibiotics9120843
Rodríguez C, Rollins-Smith L, Ibáñez R, Durant-Archibold AA, Gutiérrez A (2017) Toxins and pharmacologically active compounds from species of the family Bufonidae (Amphibia, Anura). J Ethnopharmacol 198(23): 235-254. https://doi.org/10.1016/j.jep.2016.12.021
Rosenthal GG, Ryan MR (2000) Visual and acoustic communication in non-human animals: a comparison. J Biosci 25(3): 285-290. https://doi.org/10.1007/BF02703937
Rüppel G, Gosswein E (1972) Die Schwlrme von Leucaspius delineatus (Cyprinidae. Teleostei) beiGefahr im Hellen und im Dunkeln. Z Vergleich Physiologie 76: 333-340
Schaal B, Coureaud G, Langlois D, Giniès C, Sémon E, Perrier G (2003) Chemical and behavioural characterization of the rabbit mammary pheromone. Nature 424: 68-72. https://doi.org/10.1038/nature01739
Schulte LM, Krauss M, Lötters S, Schulze T, Brack W (2015) Decoding and discrimination of chemical cues and signals: Avoidance of predation and competition during parental care behavior in sympatric poison frogs. PLoS ONE 10(7): 1-17. https://doi.org/10.1371/journal.pone.0129929
Sestito GA, Santana DJ, Garda AA, Rohr DL (2016) Parental distress call: a previously unreported defensive call in female Leptodactylus latrans (Anura, Leptodactylidae). Herpetol Notes 9: 221-225
Smiseth PT, Andrews C, Brown E, Prentice PM (2010) Chemical stimuli from parents trigger larval begging in burying beetles. Behav Ecol 21(3): 526-531. https://doi.org/10.1093/beheco/arq019.
Starnberger I, Poth D, Peram PS, Schulz S, Vences M, Knudsen J, Barej MF, Rödel KO, Walzl M, Hödl W (2013) Take time to smell the frogs: vocal sac glands of reed frogs (Anura: Hyperoliidae) contain species-specific chemical cocktails. Biol J Linn Soc 110(4): 828-838. https://doi.org/10.1111/bij.12167
Spieler M, Linsenmair KE (2001) Aggregation Behaviour of Bufo maculatus tadpoles as an antipredator mechanism. Ethology 105: 665-686. https://doi.org/10.1046/j.1439-0310.1999.00446.x
Stynoski JL (2009) Discrimination of offspring by indirect recognition in an egg-feeding dendrobatid frog, Oophaga pumilio. Anim Behav 78: 1351-1356. https://doi.org/10.1016/j.anbehav.2009.09.002
Thomas P, Vineeth Kumar TV, Reshmy V, Kumar KS, George S (2012) A mini review on the antimicrobial peptides isolated from the genus Hylarana (Amphibia: Anura) with a proposed nomenclature for amphibian skin peptides. Mol Biol Rep 39: 6943-6947. https://doi.org/10.1007/s11033-012-1521-3
Trivers RL (1972) Parental investment and sexual selection. In Campbell B (Ed) Sexual Selection and the Descent of Man. Aldine, Chicago, pp 136-179
Tyler MJ, Stone DJ, Bowie JH (1992) A novel method for the release and collection of dermal, glandular secretions from the skin of frogs. J Pharmacol Toxicol 28: 199. https://doi.org/10.1016/1056-8719(92)90004-k
Vaira M (1997) Leptodactylus bolivianus (NCN). Behavior. Herpetol Rev 28(4): 200
Valencia-Aguilar A, Guayasamin JM, Prado CPA (2021) Alloparental care in glassfrogs: males care for unrelated clutches only when associated with their own. Sci Rep 11: 1386. https://doi.org/10.1038/s41598-020-80771-7
Vaz-Ferreira R, Gehrau A (1975) Comportamiento epimelético de la rana común, Leptodactylus ocellatus (L.) (Amphibia, Leptodactylidae) I. Atención de la cría y actividades alimentarias y agresivas relacionadas. Physis Sección B 34(88): 1-14
Wells KD (2007) The Ecology and Behavior of Amphibians. The University of Chicago Press, Chicago
Wells KD, Bard, KM (1988) Parental behavior of an aquatic-breeding tropical frog. Leptodactylus bolivianus. J Herpetol 22: 361-364. https://doi.org/10.2307/1564166
Wyatt T D (2014) Pheromones and Animal Behavior: Chemical Signals and Signatures. Cambridge University Press, New York
Xu X, Lai R (2015) The Chemistry and Biological Activities of Peptides from Amphibian Skin Secretions. Chem Rev 115(4): 1760-1846. https://doi.org/10.1021/cr4006704

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Mother-offspring chemical communication and tadpole aggregation in a Neotropical foam-nesting frog

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Abstract

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Significance Statement

Introduction

Methods

Experiment 1: Attending female stimuli

Experiment 2: Intraspecific chemical stimuli

Experiment 3: School preference for related/unrelated attending female

Results

Experiment 1: Attending female stimuli

Experiment 2: Intraspecific chemical stimuli

Experiment 3: School preference for related/unrelated attending female

Discussion

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References

Supplementary Files

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