Maternal Nesting Behavior Research Articles

Nesting in Anolis Lizards: An Understudied Topic in a Well-Studied Clade

Maternal nesting behavior in oviparous species strongly influences the environmental conditions their embryos experience during development. In turn, these early-life conditions have consequences for offspring phenotypes and many fitness components across an individual’s lifespan. Thus, identifying the evolutionary and ecological causes and effects of nesting behavior is a key goal of behavioral ecology. Studies of reptiles have contributed greatly to our understanding of how nesting behavior shapes offspring phenotypes. While some taxonomic groups have been used extensively to provide insights into this important area of biology, many groups remain poorly studied. For example, the squamate genusAnolishas served as a model to study behavior, ecology, and evolution, but research focused onAnolisnesting behavior and developmental plasticity is comparatively scarce. This dearth of empirical research may be attributed to logistical challenges (e.g., difficulty locating nests), biological factors (e.g., their single-egg clutches may hinder some experimental designs), and a historical focus on males inAnolisresearch. Although there is a gap in the literature concerningAnolisnesting behavior, interest in nesting ecology and developmental plasticity in this group has grown in recent years. In this paper, we (1) review existing studies of anole nesting ecology and developmental plasticity; (2) highlight areas of anole nesting ecology that are currently understudied and discuss how research in these areas can contribute to broader topics (e.g., maternal effects and global change biology); and (3) provide guidelines for studying anole nesting in the field. Overall, this review provides a foundation for establishing anoles as models to study nesting ecology and developmental plasticity.

Temporal variation in maternal nest choice and its consequences for lizard embryos

AbstractMicrohabitat choice of nest sites is an important maternal effect that influences the survival and development of embryos in oviparous species. Embryos of many species display a high degree of plasticity in response to developmental environments, which places maternal nesting behavior under strong selective pressure, particularly in temporally changing environments. Nesting behavior varies widely across taxa that exhibit diverse reproductive strategies. The brown anole (Anolis sagrei), for example, lays one egg every 7–10 days across an extended reproductive season from April to October. This aspect of their reproduction provides an opportunity to examine temporal shifts in nesting behavior and its consequences on egg survival and offspring development under seasonally changing climatic conditions. We conducted a two-part study to quantify temporal variation in maternal nesting behavior and its effect on development of A. sagrei embryos. First, we measured nest micro-environments over the nesting season. Second, we “planted” eggs across the landscape at our field site to examine the influence of nest conditions on egg survival and hatchling phenotypes. We also incubated eggs inside chambers in the field to decouple effects of nest moisture from those of other environmental variables (e.g., temperature). Females chose nest sites with higher moisture and lower temperatures relative to what was generally available across the landscape during the nesting season. In addition, eggs exposed to relatively cool temperatures had higher hatching success, and high nest moisture increased egg survival and body condition of hatchlings. Overall, we provide evidence in the field that maternal nesting behavior facilitates offspring survival.

Spatial and temporal variation in nest temperatures forecasts sex ratio skews in a crocodilian with environmental sex determination.

Species displaying temperature-dependent sex determination (TSD) are especially vulnerable to the effects of a rapidly changing global climate due to their profound sensitivity to thermal cues during development. Predicting the consequences of climate change for these species, including skewed offspring sex ratios, depends on understanding how climatic factors interface with features of maternal nesting behaviour to shape the developmental environment. Here, we measure thermal profiles in 86 nests at two geographically distinct sites in the northern and southern regions of the American alligator's (Alligator mississippiensis) geographical range, and examine the influence of both climatic factors and maternally driven nest characteristics on nest temperature variation. Changes in daily maximum air temperatures drive annual trends in nest temperatures, while variation in individual nest temperatures is also related to local habitat factors and microclimate characteristics. Without any compensatory nesting behaviours, nest temperatures are projected to increase by 1.6-3.7°C by the year 2100, and these changes are predicted to have dramatic consequences for offspring sex ratios. Exact sex ratio outcomes vary widely depending on site and emission scenario as a function of the unique temperature-by-sex reaction norm exhibited by all crocodilians. By revealing the ecological drivers of nest temperature variation in the American alligator, this study provides important insights into the potential consequences of climate change for crocodilian species, many of which are already threatened by extinction.

Nestled in the city heat: urban nesting behavior enhances embryo development of an invasive lizard

Abstract Urbanization transforms many aspects of natural landscapes and poses many new challenges for individual survival and population persistence. Thus, urbanization provides an opportunity to examine how organisms deal with novel environmental change. Many studies provide evidence of phenotypic adaptation to urban environments, but few focus on responses during early life stages. Filling this information gap is important, because early life stages are particularly sensitive to abiotic factors, and no population is sustainable without successful embryo development. We tested the hypotheses that (i) embryos tolerate warmer temperature conditions of urbanized areas and (ii) maternal nesting behavior protects embryos from potentially lethal thermal conditions in urbanized habitats. We studied introduced populations of a subtropical lizard, Anolis cristatellus, in suburban and forested areas in Miami, Florida. In each habitat, we measured microenvironment variables for locations that females used for nesting vs. locations they did not use. We then incubated eggs from both populations under thermal conditions that mimicked used and unused sites. Nests in the suburban site were warmer than in the forest; however, in the suburban site, locations that females used were relatively cool compared with locations that were not used. We found no evidence that embryos are adapted to their respective suburban or forested thermal environments, but rather maternal nest-site choice enhanced embryo development in the suburban habitat. Maternal nesting behavior is likely an important factor for population persistence under major environmental changes, and a key contributor to the establishment and spread of invasive organisms across urbanized landscapes.

Prenatal light exposure influences gait performance and body composition in bobwhite quail chicks

Maternal nesting behavior, which includes periods of patterned inattention, provides key elements essential for avian embryonic development, including regulation of temperature and light. For example, avian research consistently shows the importance of prenatal light exposure for several developmental processes; however, this research has primarily focused on artificial light regimens (i.e. 24 hr, 0 hr light). Comparatively less is known about how exposure to naturally occurring light patterns during incubation influence motor performance, body composition (i.e. body mass, bone length), and developmental age (incubation length). Here we conducted two experiments which investigated the effects of prenatal light exposure on developmental age, body composition, and gait performance in 1-day-old bobwhite quail. Experiment 1 investigated crepuscular light exposure during the last two days of incubation under two light duration treatments (2 hr & 6 hr) compared to a 12 hr continuous light schedule. Results indicated crepuscular prenatal light experience extended the incubation period for 2 hr exposed embryos, but not for 6 hr exposed embryos and negatively influenced postnatal body composition and postnatal gait performance when compared to 12 hr continuous light embryos. Experiment 2 examined the influence of prenatal light duration (2 hr vs 6 hr) and light presentation (crepuscular vs sporadic). Results demonstrated sporadic light presentation improved gait performance in 2 hr exposed hatchlings, but not 6 hr exposed hatchlings, improved body composition in 6 hr exposed hatchlings, but not 2 hr exposed hatchlings, and did not alter incubation length when compared to crepuscular light counterparts. This study provides further evidence for the importance of maternally regulated sensory stimulation during the prenatal period on early postnatal motor development.

The influence of maternal nesting behaviour on offspring survival: evidence from correlational and cross-fostering studies

The maternal effect of nesting behaviour is important in oviparous species because choice of microhabitat (e.g. shade cover, temperature) can determine the environment in which embryos develop. In turn, this maternal choice can influence developmental trajectories and offspring phenotypes and survival. We studied maternal nesting behaviour in a western painted turtle, Chrysemys picta, population in northern Idaho, U.S.A. During 2013–2016, we examined maternal choice of nest microhabitat and used correlational data to quantify consequences on egg survival. In 2017, we conducted a cross-fostering experiment to decouple the effects of intrinsic maternal effects from extrinsic environmental factors on egg survival, while simultaneously manipulating the level of nest shade cover and distance from water using artificial nests. Females chose nest sites that were more open and warmer than randomly available habitat. Additionally, of three nesting areas, the coolest area with the most shade cover was used least by nesting females. Egg survival was associated with nest temperature in some, but not all, years. In the cross-fostering experiment, egg survival did not differ between natal and foster eggs, but was greater in maternal nests than in artificial nests. Additionally, egg survival increased with canopy openness and minimum nest temperature, especially for eggs in artificial nests. Overall, these results suggest that females select nesting conditions (warm and open nest sites) that positively affect hatching success.

Maternal nest-site choice does not affect egg hatching success in an invasive turtle population

Abstract Embryos of many oviparous organisms are sensitive to conditions within their nest, and maternal nesting behaviours could potentially buffer embryos from suboptimal developmental environments. Thus, maternal behaviour could influence how organisms respond to novel environments. We studied an invasive population of red-eared slider turtles (Trachemys scripta elegans) in Oregon, USA to determine if maternal choice of nest microhabitat facilitates development in environments outside the native range. We show that females nested on relatively shallow slopes and used open microhabitats compared to random sites. However, by splitting eggs from clutches between maternally-chosen nests and randomly-selected “nest sites”, we show that egg hatching success was low overall (32.8%) and was not influenced by maternal nest-site choice. Our study highlights the importance of understanding how maternal nesting behaviour and survival during early life stages (e.g., embryos) might contribute to the long-term persistence of invasive populations, which is important for their proper management.

Maternal nesting behaviour in city dragons: a species with temperature-dependent sex determination

Abstract Urban environments present some of the greatest challenges to species survival. This is particularly true for species that exhibit thermally sensitive traits, such as temperature-dependent sex determination (TSD). This is because urban environments not only present species with entirely novel ecosystems, but species will also experience increased temperatures. These temperature increases may result not only in offspring mortality, but also skewed population sex ratios. To persist in cities, urban dwellers with TSD will therefore need to adjust the temperature of the nesting environment, either through phenotypic plasticity or rapid evolution through natural selection. Here, we investigate the nesting ecology of a long-lived, urban dwelling reptile, the eastern water dragon (Intellagama lesueurii), to understand how a TSD species may respond to urban environments. Based on data collected from 72 nests over 2 nesting seasons, we show that city dragons not only dug significantly deeper nests than previously observed across their natural riparian habitat, but also nested in novel substrates. Furthermore, we observed a behaviour not previously described in this species, where mothers travel outside of their core home range to nest. This excursion behaviour potentially represents a greater maternal investment and is linked to the selection of specific microhabitats.

Temperature-Dependent Sex Determination under Rapid Anthropogenic Environmental Change: Evolution at a Turtle's Pace?

Organisms become adapted to their environment by evolving through natural selection, a process that generally transpires over many generations. Currently, anthropogenically driven environmental changes are occurring orders of magnitude faster than they did prior to human influence, which could potentially outpace the ability of some organisms to adapt. Here, we focus on traits associated with temperature-dependent sex determination (TSD), a classic polyphenism, in a model turtle species to address the evolutionary potential of species with TSD to respond to rapid climate change. We show, first, that sex-ratio outcomes in species with TSD are sensitive to climatic variation. We then identify the evolutionary potential, in terms of heritability, of TSD and quantify the evolutionary potential of 3 key traits involved in TSD: pivotal temperature, maternal nest-site choice, and nesting phenology. We find that these traits display different patterns of adaptive potential: pivotal temperature exhibits moderate heritable variation, whereas nest-site choice and nesting phenology, with considerable phenotypic plasticity, have only modest evolutionary potential to alter sex ratios. Therefore, the most likely response of species with TSD to anthropogenically induced climate change may be a combination of microevolution in thermal sensitivity of the sex-determining pathway and of plasticity in maternal nesting behavior.

Nesting ecology and offspring recruitment in a long‐lived turtle

The role of early life stages (eggs, neonates, and juveniles) for population persistence in long‐lived organisms is thought to be minor. However, few long‐term data sets are available to test this assumption. Variation in vital rates over space and time and the potential for the success of early life stages to shape adult reproductive behavior evolutionarily suggest that more thorough consideration of these life stages is necessary. In particular, the impact of climatic variation on early life‐stage recruitment is not well understood. Furthermore, predation occupies a significant role in theoretical models of population dynamics, but its impact on populations through variable vital rates of early life stages is unknown. Maternal nest‐site choice, an important component of nesting ecology, may influence many offspring traits and respond to selection to optimize offspring success. Overall, we have limited information regarding the long‐term patterns of natural fluctuations in the nesting ecology and hatchling recruitment of populations of long‐lived organisms.The research site for this ongoing long‐term project is on an island in the Mississippi River near Thomson, Illinois, USA. Painted turtles (Chrysemys picta) have been studied extensively at this location since 1989 to examine the ecology and potential demographic consequences of nest‐site choice and depredation, with the aim of understanding the evolution of maternal nesting behavior and its effects on offspring phenotype. We monitored the site every day of the nesting season each year to record nesting and depredation events. The data presented here include nesting phenology, nest vegetation cover, total number of nesting events, clutch size, depredation, and hatchling survival.Portions of this data set have been used to address related questions in ecology and evolutionary biology. In particular, climatic variation influences the probability of nest depredation events. Such events are typically nonrandom, primarily occurring adjacent to habitat edges. Because habitat edges may have atypical vegetation composition and vegetation influences nest temperature, such nonrandom depredation could influence offspring recruitment and, hence, population structure. Given the unique scope and accessibility of this data set, researchers and teachers should find it to be a valuable empirical resource for exploring important facets of nesting ecology and hatchling recruitment in a wild population of a long‐lived species.The complete data sets corresponding to abstracts published in the Data Papers section of the journal are published electronically in Ecological Archives at 〈http://esapubs.org/archive〉. (The accession number for each Data Paper is given directly beneath the title.)

Effect of 2,4-dichlorophenoxyacetic acid on rat maternal behavior

Exposure to 2,4-dichlorophenoxyacetic acid (2,4-D) has several deleterious effects on the nervous system such as alterations in the concentrations of neurotransmitters in the brain and/or behavioral changes, myelination rate, ganglioside pattern [Bortolozzi, A., Duffard, R., Antonelli, M., Evangelista de Duffard, A.M., 2002. Increased sensitivity in dopamine D(2)-like brain receptors from 2,4-dichlorophenoxyacetic acid (2,4-D)-exposed and amphetamine-challenged rats. Ann. N.Y. Acad. Sci. 965, 314-323; Duffard, R., García, G., Rosso, S., Bortolozzi, A., Madariaga, M., DiPaolo, O., Evangelista de Duffard, A.M., 1996. Central nervous system myelin deficit in rats exposed to 2,4-dichlorophenoxyacetic acid throughout lactation. Neurotoxicol. Teratol. 18, 691–696; Evangelista de Duffard, A.M., Orta, C., Duffard, R., 1990. Behavioral changes in rats fed a diet containing 2,4-dichlorophenoxyacetic butyl ester. Neurotoxicology 11, 563–572; Evangelista de Duffard, A.M., Bortolozzi, A., Duffard, R.O., 1995. Altered behavioral responses in 2,4-dichlorophenoxyacetic acid treated and amphetamine challenged rats. Neurotoxicology 16, 479–488; Munro, I.C., Carlo, G.L., Orr, J.C., Sund, K., Wilson, R.M. Kennepohl, E. Lynch, B., Jablinske, M., Lee, N., 1992. A comprehensive, integrated review and evaluation of the scientific evidence relating to the safety of the herbicide 2,4-D. J. Am. Coll. Toxicol. 11, 559–664; Rosso et al., 2000], and its administration to pregnant and lactating rats adversely affects litter growth and milk quality. Since normal growth of the offspring depends on adequate maternal nursing and care, we evaluated the effect of 2,4-D on rat maternal behavior as well as the dam's monoamine levels in arcuate nucleus (AcN) and serum prolactin (PRL) levels. Wistar dams were exposed to the herbicide through the food from post partum day (PPD) 1 to PPD 7. Dams were fed either with a 2,4-D treated diet (15, 25 or 50 mg 2,4-D/kg/day bw) or with a control diet. We observed that maternal nesting behavior was not modified by 2,4-D treatment. However, mother–pup interactions, specially the nursing behavior, were altered. Retrieval, crouching and licking of pups were reduced or suspended after 2,4-D treatment. We also observed an increase in the latency of retrieval and crouching in the dams treated with the herbicide. Dams showed movement along cage peripheries, food consumption during the light phase and high self-grooming. In addition of the deficits observed in maternal behavior parameters, increased catecholamine levels and a drastic decrease in indolamine levels in the AcN of treated dams were determined. Serum PRL levels were also diminished by 62%, 68% and 70% with respect to control dams in the 15, 25 and 50 mg 2,4-D/kg bw treated dams, respectively. In conclusion, exposure to 2,4-D during the first post partum days produced changes in maternal behavior, serum prolactin and monoamine levels in the AcN of treated dams.

Nest site choice compensates for climate effects on sex ratios in a lizard with environmental sex determination

Theoretical models suggest that in changing environments natural selection on two traits, maternal nesting behaviour and pivotal temperatures (those that divide the sexes) is important for maintaining viable offspring sex ratios in species with environmental sex determination (ESD). Empirical evidence, however, is lacking. In this paper, we provide such evidence from a study of clinal variation in four sex-determining traits (maternal nesting behaviour, pivotal temperatures, nesting phenology, and nest depth) in Physignathus lesueurii, a wide-ranging ESD lizard inhabiting eastern Australia. Despite marked differences in air and soil temperatures across our five study sites spanning 19° latitude and 1200 m in elevation, nest temperatures did not differ significantly among sites. Lizards compensated for climatic differences chiefly by selecting more open nest sites with higher incident radiation at cooler sites. Clinal variation in the onset of nesting also compensated for climatic differences, but to a lesser extent. There was no evidence of compensation through pivotal temperatures or nest depth. More broadly, our results extend to the egg stage the life history prediction that behaviour is the chief compensatory mechanism for climatic differences experienced by species spanning environmental extremes. Furthermore, our study was unique in revealing that nest site choice influenced mainly the daily range in nest temperatures, rather than mean temperatures, in a shallow-nesting reptile. Finally, indirect evidence suggests that the cue used by nesting lizards was radiation or temperature (through basking or assessing substrate temperatures), not visual detection of canopy openness. We conclude that maternal nesting behaviour and nesting phenology are traits subject to sex ratio selection in P. lesueurii, and thus, must be considered among the repertoire of ESD species for responding to climate change.

Repeatability of microenvironment-specific nesting behaviour in a turtle with environmental sex determination

Evolutionary thermal adaptation is increasingly being elucidated in a variety of systems. However, one of the most striking examples, temperature-dependent sex determination (TSD) in reptiles, has proven stubbornly difficult to decipher. Theoretical models suggest that selection on and heritable variation in thermal sensitivity of embryonic sex determination and maternal behavioural choice of thermal qualities of nest sites control the microevolutionary potential of TSD. To begin addressing this important issue, we conducted a multiyear field study of nesting behaviour in painted turtles (Chrysemys picta), which display TSD. We detected a significant field repeatability for overstory vegetation cover around nests at oviposition, a trait that is correlated inversely with nest temperature during embryonic sex determination and positively with offspring sex ratio (percentage of male). Neither clustered nesting nor individual spatial repeatability in nest site choice caused this striking pattern. Instead, females consistently preferred nest environments with particular quantities of overstory vegetation cover. These findings confirm a crucial assumption of models concerning the microevolution and adaptive significance of TSD in reptiles. The results also indicate that this system may be able to evolve via long-term maternal nesting behaviour in response to skewed sex ratios caused by environmental perturbations, such as gradual long-term climate change.

Development and growth of Planigale tenuirostris (Marsupialia: Dasyuridae) in the laboratory.

Development and growth of Planigale tenuirostris are described with data for three litters bred in the laboratory. Growth curves were constructed for the length of head plus body, tail, head and foot; the width of head and scrotum and the body weight for the period from birth to 200 days old. A regression equation is given that predicts age during the first 30 days of life. The young of P. tenuirostris first detached from the teats at 36 days, had their eyes open at 51 days and were weaned at 95 days. Field data on development are in agreement with those for the laboratory individuals. Features of development, growth and maternal nesting behaviour are compared with those known for other small dasyurids.

Thermoendocrine influences on maternal nesting behavior in rats.

Adrenalectomy-ovariectomy (adex-ovex) of mother rats resulted in prolonged nest bouts with their young. Glucocorticoid, but not progesterone or aldosterone, replacement therapy to adex-ovex dams limited the duration of maternal nesting bouts by successfully restoring the chronic vulnerability of these mother rats to the acute thermal consequences of huddling with the young. This vulnerability appeared to be due to a chronic elevation of maternal temperature. When the heat load of hormone-disrupted mothers was chronically elevated, the dams were subject to an acute rise in temperature while huddling with their young, and nest bouts were curtailed.

Effects of postnatal alcohol exposure on maternal nesting behavior in the rat

Seven female Wistar rats were fed a liquid diet containing Sustagen and ethanol through Days 1–17 of lactation. Six control females were pair-fed an identical liquid diet except for isocaloric substitution of sucrose for ethanol. Continuous monitoring of maternal nesting behavior, employing automated nesting chambers, indicated that the mothers fed ethanol spent more time on the nest nursing their young than the pair-fed controls during the middle of the observation period. This increase in nesting time may be due to a decrease in activity in the ethanol-fed mothers or due to greater heat loss in their pups, allowing them to remain longer on the nest. This increased nesting time occurs when the pups’ motor effectiveness and exploratory drive are developing, and may account for the long-term behavioral changes seen in the pups.

An inexpensive system for continuously recording maternal behavior in the laboratory rat

A system is described for the continuous recording of time spent on the nest by mother rats. Accurate estimates of nursing time are obtained by limiting the space available for nesting and making food and water available only outside of the nesting area. The apparatus may also be used to monitor preparturient circadian activity, and to estimate the time of parturition. It is suggested that continuous monitoring of maternal nesting behavior be an important adjunct to experiments involving manipulation of the mother or litter.