Nest, but Not Egg, Fidelity in a Territorial Salamander

Egg recognition and subsequent egg brooding are costly forms of parental investment in many species of vertebrates. Life history factors, such as coloniality or risk of brood parasitism, may constrain egg recognition in vertebrates. Female red-backed salamanders ( Plethodon cinereus ) from my study site are territorial and do not share nest sites with other females. They are terrestrial and neither they nor their eggs are likely to be displaced by environmental factors such as flooding. I experimentally tested, in the laboratory, the hypothesis that female red-backed salamanders can discriminate between their own eggs and the eggs of unfamiliar females. Each female was allowed to move about a test chamber containing two clutches of eggs, one clutch with which it was found in the forest and one that had been found with a distant female. Most females remained with one clutch of eggs, which they brooded during the entire observation period. However, they did not significantly prefer to brood their own eggs over the eggs of another female. In a corollary field experiment, I tested whether brooding females that were displaced 1 m from their nest sites would return to their territories and commence brooding behaviour within 3 d. All 10 displaced females returned to their own nest within this time period and were found brooding their eggs. Because female red-backed salamanders at my study site do not tend to share nest sites with other females and because their eggs remain in stationary nests, selection may not have favoured egg recognition. However, the results suggest that female salamanders indirectly recognize their own eggs by actively recognizing their territorial nest sites.     

Egg discrimination in the Australian reed warbler (Acrocephalus australis): rejection response toward model and conspecific eggs depending on timing and mode of artificial parasitism

In a coevolutionary arms race between an interspecific broodparasite and its host species, both are expected to evolveadaptations and counteradaptations. We studied egg discriminationin the Australian warbler (Acrocephalus australis). This speciesis currently not significantly parasitized by the seven speciesof cuckoo for which it is a suitable host. However, experimentalbrood parasitism in the warbler revealed a fine tuned egg discriminationresponse towards non-mimetic and conspecific eggs, the firstsuch evidence in an Australian passerine: (1) non-mimetic eggswere significantly more often rejected than conspecific eggs;(2) only non-mimetic dummy eggs were rejected selectively,whereas rejection of conspecific eggs entailed a rejectioncost; (3) replacement of a host's egg with a conspecific eggduring egg laying resulted in a significantly higher rejectionrate than after the day of clutch completion; (4) by contrast,rejection rate after addition of a conspecific egg was independentof nest stage; (5) conspecific eggs introduced into a clutchduring the egg laying period led to a significantly highernest desertion rate and a lower egg ejection rate than afterthe day of clutch completion; and (6) addition of a conspecificegg led to egg ejection while egg replacement with a conspecificegg led to nest desertion. The fact that this species respondsdifferentially toward different modes of artificial parasitismsuggests that its egg discrimination has evolved to minimizethe costs of rejection and parasitism. The ability to rejecthighly mimetic conspecific eggs may explain the current paucityof brood parasitism in this species. The significance of thisfor brood parasite-host coevolution is discussed.     

Population and Species Divergence of Chemical Cues that Influence Male Recognition of Females in Desmognathine Salamanders

Growing evidence indicates that males may be more discriminating of mating partners than often has been assumed. In the North American Ocoee dusky salamander, Desmognathus ocoee (Plethodontidae: Desmognathinae), sexual incompatibility among conspecific populations is high in encounters staged in the laboratory, at least in part because males fail to recognize ‘other’ females as appropriate targets for courtship. I used Y-mazes to test the hypothesis that males of D. ocoee discriminate between substrate-borne chemical cues produced by ‘own’ (homotypic) and ‘other’ (heterotypic) females. Males of four populations discriminated in favor of substrates soiled by homotypic females over clean (control) substrates (expt 1), suggesting that females produce chemical cues of sociosexual significance to males. Furthermore, males from these populations discriminated in favor of substrates soiled by homotypic females vs. substrates soiled by heterotypic females (expt 2), both conspecific and heterospecific (D. carolinensis and D. orestes). Thus, differences among populations and species in female chemical cues appear to affect the chemotactic responses of males. I suggest that, together with differences in behavioral signals and responses exhibited during courtship, differences in female chemical cues likely contribute to sexual incompatibility among populations and taxa of desmognathine salamanders.     

Responses of Black-headed Gulls Larus ridibundus to conspecific brood parasitism

Conspecific brood parasitism in birds occurs when a female inserts her egg into the clutch of her own species. If successful, i.e. the parasitic egg is accepted by the host, then the host female or pair rears the offspring of the parasite. In the present study, we studied natural conspecific brood parasitism in Black-headed Gulls (Larus ridibundus), and conducted series of the experiments with mimetic (conspecific) and non-mimetic (conspecific painted light blue) eggs to explore responses of the tested pairs towards these alien eggs. The natural parasitism rate was 10% and the probability of being parasitized significantly increased with nest density. Experimentally parasitized pairs rejected both types of experimental eggs at a similar rate: 14.3 % for mimetic and 25.5% for non-mimetic within 2 days. Non-mimetic eggs were more selectively rejected than mimetic eggs. The relationships between the probability of egg rejection (dependent variable) and predictor (independent) variables were examined by fitting generalized linear models. Contrast and intraclutch variation in ground color and spotting pattern and the volume of the egg had no significant effect on rejection behavior in either non-mimetic or mimetic eggs. However, nest density significantly positively affected rejection behavior of the Black-headed Gulls in both non-mimetic and mimetic treatments.     

Responses of a plethodontid salamander to conspecific and congeneric intruders

After inhabiting their home sites for a few days, both males and females of the salamander Desmognathus monticola directed agonistic behaviour toward intruding salamanders. Resident D. monticola were significantly more aggressive toward D. fuscus intruders than toward conspecific ones, although both conspecific and congeneric intruders were frequently attacked. Responses of D. monticola residents were independent of sex, and no difference was found in the behaviour of residents toward conspecific male and female intruders. Small D. fuscus intruders were attacked and injured more frequently than similar-sized D. monticola intruders and, in general, smaller-sized salamanders were the victims of aggressive attacks more frequently than larger ones. The proportions of bites on the head and tail of intruders were similar, although injuries were much more frequent to the tail than to the head. This species-related and size-related agonistic behaviour may be functional in maintaining the spatial distribution of species in communities of Desmognathus salamanders.     

Evidence of selection for egg crypsis in conspicuous nests

ABSTRACT The value of egg coloration as crypsis, once accepted as a general principle, has recently been questioned because most experiments have failed to show that egg coloration deters predation. The nest‐crypsis hypothesis postulates that, among species that build conspicuous nests, selection for egg crypsis is relaxed or absent because visually searching predators detect nests prior to eggs. I tested the nest‐crypsis hypothesis using the large, relatively conspicuous nests of American Robins (Turdus migratorius), and eggs that differed markedly in color that were collected from the nests of Red‐winged Blackbirds (Agelaius phoeniceus), Brewer's Blackbirds (Euphagus cyanocephalus), and Yellow‐headed Blackbirds (Xanthocephalus xanthocephalus). Each nest (N= 22) received a clutch of each species during three sequential predation trials that were 16 d in duration. The order of clutch presentation was randomized for each nest. Survival trends for Brewer's and Yellow‐headed Blackbirds were similar, and higher than those for clutches of Red‐winged Blackbirds. By the end of trials, overall survival of the three clutch types was roughly equivalent. However, clutches of Red‐winged Blackbird eggs, the most conspicuous egg type to the human eye, were discovered sooner by predators. Because the experimental design controlled for effects of nest crypsis, nest location, and nest size, this difference in egg survival can be attributed to differences in egg pigmentation. Thus, my results support a role for egg coloration as camouflage in conspicuous nests.     

How to Spot a Stranger's Egg? A Mimicry‐Specific Discordancy Effect in the Recognition of Parasitic Eggs

Egg discrimination by hosts is an antiparasitic defence to reject foreign eggs from the nest. Even when mimetic, the presence of brood parasitic egg(s) typically alters the overall similarity of all eggs in a clutch, producing a discordant clutch compared to more homogenous clutches of composed only of hosts’ own eggs. In multiple parasitism, the more foreign eggs are laid in the nest, the more heterogeneous the overall clutch appears. Perceptual filters and recognition templates cannot explain the known pattern of lower rejection rates of foreign eggs in multiple vs. single parasitism. We therefore assessed the role of clutch homogeneity and manipulated the colour of one or more eggs in the clutches of great reed warbler (Acrocephalus arundinaceus) hosts of common cuckoos (Cuculus canorus). Varying the colours of both the majority and the minority eggs caused predictable shifts in the rejection of the focal egg(s), and ejection rates of the minority egg colour consistently increased but only when it belonged to a more mimetic egg colour, relative to the less mimetic colour of majority eggs. The results imply that in addition to sensory filters, and template‐based cognitive decision rules, discordancy‐based rejection is affected by the overall clutch appearance and interacts with specific colours varying in the extent of mimicry, to contribute to the recognition decisions of hosts to reject parasitic eggs.     

Do Brooding Pythons Recognize their Clutches? Investigating External Cues for Offspring Recognition in the Children's Python,Antaresia childreni

Parental care provides substantial benefits to offspring but exacts a high cost to parents, necessitating the evolution of offspring recognition systems when the risk of misdirected care is high. In species that nest, parents can use cues associated with the offspring (direct offspring recognition) or the nest (indirect offspring recognition) to reduce the risk of misdirected care. Pythons have complex parental care, but a low risk of misdirected care. Thus, we hypothesized that female Children's pythons (Antaresia childreni) use indirect cues to induce and maintain brooding behavior. To test this, we used a series of five clutch manipulations to test the importance of various external brooding cues. Contrary to our hypothesis, we found that female A. childreni are heavily internally motivated to brood, needing only minimal external cues to induce and maintain egg‐brooding behavior. Females were no more likely to brood their own clutch in the original nest as they were to brood a clutch from a conspecific, a pseudoclutch made from only the shells of a conspecific, or their clutch in a novel nest. The only scenario where brooding was reduced, but even then not eliminated, was when the natural clutch was replaced with similarly sized stones. These results suggest that egg recognition in pythons is similar to that of solitary‐nesting birds, which have similar nesting dynamics.     

The modelling of avian visual perception predicts behavioural rejection responses to foreign egg colours

How do birds tell the colours of their own and foreign eggs apart? We demonstrate that perceptual modelling of avian visual discrimination can predict behavioural rejection responses to foreign eggs in the nest of wild birds. We use a photoreceptor noise-limited colour opponent model of visual perception to evaluate its accuracy as a predictor of behavioural rates of experimental egg discrimination in the song thrush Turdus philomelos. The visual modelling of experimental and natural eggshell colours suggests that photon capture from the ultraviolet and short wavelength-sensitive cones elicits egg rejection decisions in song thrushes, while inter-clutch variation of egg coloration provides sufficient contrasts for detecting conspecific parasitism in this species. Biologically realistic sensory models provide an important tool for relating variability of behavioural responses to perceived phenotypic variation.     

Does maternal care evolve through egg recognition or directed territoriality?

The mechanism that facilitates the evolution of maternal care is ambiguous in egg‐laying terrestrial vertebrates: does the ability of mothers to recognize their own eggs lead them under some circumstances to begin providing care or can maternal care evolve from simply being in close proximity to the eggs (e.g. through territorial behaviour)? This question is difficult to answer because in most species, parental care is either absent altogether or present; in only a few species we have the opportunity to observe intraspecific variation in the expression of parental care. We studied a population of long‐tailed skinks (Eutropis longicaudata) in which females have recently evolved maternal care from a noncaring state. Females on Orchid Island, Taiwan, remain with their eggs during incubation and when doing so, actively deter egg predation by egg‐eating snakes (Oligodon formosanus); in all other populations, females lack post‐ovipositional maternal care. Nest‐guarding females on Orchid Island (i) showed antipredator behaviours only in the original nest site in which they laid eggs, even after we removed all of the eggs or substituted them with those of a conspecific; (ii) protect any eggs present inside the original nest site (even when the eggs belong to a conspecific); and (iii) develop this behaviour while gravid (i.e. prior to laying eggs). This supports the hypothesis that long‐tailed skinks cannot recognize their own eggs, suggesting that maternal care is a directed form of territoriality only expressed towards egg‐eating snakes and only during reproduction. Nest guarding is among the most primitive forms of parental care, and the recent evolution of this behaviour in a single population provides insight into one of the mechanisms by which parental care can originate in terrestrial vertebrates.     

Failed species,innominate forms,and the vain search for species limits: cryptic diversity in dusky salamanders (Desmognathus) of eastern Tennessee

Cytochrome B sequences and allozymes reveal complex patterns of molecular variation in dusky salamander (Desmognathus) populations in eastern Tennessee. One group of allozymically distinctive populations, which we refer to as the Sinking Creek form (SCF), combines morphological attributes of Desmognathus fuscus with cytB sequences characteristic of Desmognathus carolinensis. This form is abruptly replaced by D. fuscus just north of Johnson City, TN with no evidence of either sympatry or gene exchange. To the south, allozymic markers indicate a broad zone of admixture with populations characterized by distinct cytB sequences and that may or may not be ultimately referable to Desmognathus conanti. A third distinctive group of populations, which we refer to as the Lemon Gap form (LGF), occurs in the foothills of the Great Smoky and southern Bald Mountains and exchanges genes with Desmognathus santeetlah along the escarpment of the Great Smokies, D. carolinensis in the southern Bald Mountains, and populations of a different haplotype clade in the Ridge and Valley. We treat all these as innominate forms that may represent “failed species,” recognizing that it may never be possible to reconcile species limits with patterns of phylogeny, morphology, and gene exchange in these salamanders.     

The use of volatile cues in recognition of kin eggs by predatory mites

1. Several animal species are known to distinguish between their own eggs and eggs of unrelated conspecifics. However, the cues involved in this discrimination are often unknown. These cues were studied using the predatory mite Gynaeseius liturivorus Ehara.
2. Adult females of these predatory mites oviposit in clusters and avoid oviposition close to eggs laid by other females, resulting in reduced cannibalism between offspring. Because predatory mites are blind, it was tested whether volatiles of eggs were used as a cue for egg recognition.
3. Adult female predatory mites were offered volatile cues of their own eggs and of unrelated conspecific eggs, and females were prevented from contacting the eggs. Predatory mites oviposited closer to their own eggs than to unrelated eggs. This preference was observed even when one own and one unrelated egg were offered as a volatile source.
4. These results suggest that adult female predatory mites can determine kinship using volatiles released from the eggs.

     

Egg ejection cost can limit defence strategies against brood parasitism

A cost associated with the evolution of antiparasite strategies is the failure to recognize parasitic eggs, leading the host to evict its own eggs. However, there is evidence that birds recognize their own eggs through imprinting. This leads to the question of why birds accept parasitic eggs if such eggs can be identified. Here, we tested whether egg ejection per se can be costly due to increased predation risk to the remaining clutch and whether olfactory or visual cues of egg ejection increase predation. We carried out three field experiments to answer the following questions: (a) Does ejecting an egg increase nest predation risk? (b) Does the presence of olfactory cues, such as the smell of a broken egg, increase nest predation risk? And (c) Does the presence of visual cues, such as an egg shell below the nest, increase nest predation risk? We found evidence that egg ejection increases nest predation and that olfactory cues alone also increase nest predation. The presence of visual cues did not change predation rates. These data indicate that egg ejection is costly for both host and parasitic eggs that may remain in the nest. Our results suggest why host and parasite eggs are commonly found within the same nests, despite the possibility that hosts recognize and could possibly eject the parasite’s egg.     

Incubation capacity and clutch size determination in two calidrine sandpipers: a test of the four-egg threshold

Several groups of vertebrate taxa, including shorebirds, are unusual in that they produce a fixed number of offspring. The aim of this study was to examine whether the incubation capacity of western sandpipers (Calidris mauri) and semipalmated sandpipers (C. pusilla) limits their maximum clutch size to four eggs. Experimental enlargement of clutch size had no effect on rates of nest abandonment, nest attendance or loss of body mass by incubating sandpipers. The duration of incubation was significantly longer for enlarged five-egg nests, and there were trends towards increased partial clutch loss and asynchrony at hatch, but overall hatching success was unaffected by experimental egg number. I conclude that small, calidrine sandpipers with biparental care are able to compensate for an additional egg in an enlarged nestbowl, despite the constraints of conically shaped eggs and two brood patches. Possibly, shorebirds do not lay more than a fixed clutch size of four eggs because selection on factors acting during egg production or brood-rearing is more important in regulating offspring number. Received: 20 June 1996 / Accepted: 30 September 1996     

Egg Coloration and Recognition of Conspecific Brood Parasitism in Eastern Bluebirds

Individual eastern bluebird (Sialia sialis) females produce clutches of eggs with unique coloration and older females and females in better body condition lay more pigmented blue‐green eggs. Conspecific brood parasitism in this species is not uncommon and bluebirds occasionally reject what appear to be normal eggs by moving them to the periphery of the nest. I used UV‐visual reflectance spectrometry to objectively measure coloration of eggs and nest material. To estimate the conspicuousness of the trait, I calculated the contrast between eggs and background nest material. I found high achromatic and chromatic contrast between the coloration of eggs and of the nests, suggesting that bluebird eggs are highly conspicuous. To test the hypothesis that expression of blue‐green coloration eggs facilitates recognition of eggs laid by conspecific brood parasites, I cross‐fostered individual eggs into host nests during egg laying and monitored the fate of those eggs. I found no support, however, for the hypothesis that egg coloration facilitates discrimination of parasitic eggs from host eggs.     

How avian incubation behaviour influences egg surface temperatures: relationships with egg position,development and clutch size

While understanding heat exchange between incubating adults and their eggs is central to the study of avian incubation energetics, current theory based on thermal measurements from dummy eggs reveals little about the mechanisms of this heat exchange or behavioural implications for the incubating bird. For example, we know little about how birds distribute their eggs based on temperature differences among egg positions within the nest cup. We studied the great tit Parus major, a species with a large clutch size, to investigate surface cooling rates of individual eggs within the nest cup across a range of ambient temperatures in a field situation. Using state‐of‐the‐art portable infrared imaging and digital photography we tested for associations between egg surface temperature (and rate of cooling) and a combination of egg specific (mass, shape, laying order, position within clutch) and incubation specific (clutch size, ambient temperature, day of incubation) variables. Egg surface temperature and cooling rates were related to the position of the eggs within the nest cup, with outer eggs being initially colder and cooling quicker than central eggs. Between foraging bouts, females moved outer eggs significantly more than centrally positioned eggs. Our results demonstrate that females are capable of responding to individual egg temperature by moving eggs around the nest cup, and that the energy cost to the female may increase as incubation proceeds. In addition, our results showing that smaller clutches experience lower initial incubation temperatures and cool quicker than larger clutches warrant further attention for optimal clutch size theory and studies of energetic constraints during incubation. Finally, researchers using dummy eggs to record egg temperature have ignored important elements of contact‐incubation, namely the complexity of how eggs cool and how females respond to these changes.     

Differential Kin Discrimination by Red-spotted Newts (Notophthalmus viridescens) and Smooth Newts (Triturus vulgaris)

In organisms lacking parental care or when eggs of more than one female are layed together, parents preferentially tend to avoid eating their own offspring. In some species of newts (Caudata: Salamandridae), there is no parental care and cannibalism of eggs and larvae occurs when philopatric adults remain in the pond throughout the breeding season where eggs and larvae develop. Kin discrimination by both adult newts and larvae would be expected to occur during the breeding season as it would enable individuals to benefit from the nutrients obtained from eating eggs and larvae while they avoid eating close relatives. The effects of kinship on cannibalism of eggs and larvae were examined in two species of newts. In separate, but similar, paired behavioral trials adult female red-spotted newts, Notophthalmus viridescens, and smooth newts, Triturus vulgaris, were allowed to consume their own egg or an egg from another female. Female red-spotted newts, but not smooth newts, preferred to eat eggs of other females rather than their own, and overall smooth newts were ‘reluctant’ to eat conspecific eggs. To test for ontogenetic shifts in discrimination abilities, additional experiments were performed with adult female red-spotted newts paired with their own larvae and a larva from another female. In addition, the effects of kinship on the attraction or repulsion of larvae was also studied in red-spotted newts. Females showed no significant discrimination abilities during acts of cannibalism on larvae. Larvae spent similar amounts of time with siblings and non-siblings. These results suggest that the ability of adult newts to discriminate among eggs varies between species and that the elicitation of a kin-discrimination response may be context-dependent. For red-spotted newts, there was no evidence of discrimination abilities within and between other life-history stages.     

The use of ultrasonography to assess reproductive investment and output in pythons

Reproductive investment and output are integral fitness components, often incorporated into life‐history trade‐off models and important to population dynamics. The trade‐offs associated with reproduction can be dramatic in species such as snakes that make especially large investments into reproduction. Unfortunately, traditional methods used to determine reproductive investment and output are effective in many (but not all) situations. Thus, we used portable ultrasonography to serially estimate reproductive investment and reproductive output in three python species that exhibit significant variation in phylogeny, geographic range, body size, egg size, and clutch size: ball pythons (Python regius), Children's pythons (Antaresia childreni), and water pythons (Liasis fuscus). At each time point of measurement (range: 1–49 days pre‐oviposition), ultrasound estimates of viable clutch size were highly accurate in all three species. However, ultrasound estimates of mean viable egg mass, and thus viable clutch mass, significantly differed from the actual values (range: 23–73% error). Interestingly, this error was considerably smaller as females approached oviposition, suggesting that female pythons transfer a significant amount of water into their eggs during the week before oviposition. Thus, water balance during late‐stage egg development may be an integral part of reproductive success. The results obtained in the present study form the foundation for future assessments of reproductive investment, and also provide insight into the use of ultrasound technology to assist such efforts. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 103 , 772–778.     

Influence of Shape on Egg Discrimination in American Robins and Gray Catbirds

The eggs of some obligate brood parasites are more spherical than the eggs of their non‐parasitic relatives and hosts, which contributes to the increased strength of their shells. We examined whether egg shape, including the more spherical shape of brown‐headed cowbird eggs (Molothrus ater), influenced egg discrimination in American robins (Turdus migratorius) and gray catbirds (Dumetella carolinensis). We added a series of artificial objects to robin and catbird nests that varied in shape from a control host egg, a rounded, cowbird‐like egg, to odd‐shaped objects. Real cowbird eggs were significantly more spherical than catbird and robin eggs, which confirmed a potential cue for egg recognition. Object shape significantly influenced the probability of rejection and time to rejection in both robins and catbirds. However, rounded eggs and spheres were rejected infrequently and at frequencies similar to control eggs. Therefore, the shape of a brood parasite's egg does not appear to influence egg discrimination in these two rejecters. Robins and catbirds rejected significantly more odd‐shaped objects than egg‐shaped objects and odd‐shaped objects were rejected significantly sooner than egg‐shaped objects. The rejection of odd‐shaped objects likely represents an expression of nest‐sanitation behaviour where debris is removed from the nest. By comparison with other studies of accepters of cowbird eggs, robins and catbirds appear to reject higher proportions of odd‐shaped objects, which suggests they may have more refined abilities to discriminate against foreign objects in their nests.     

Nest Sanitation as the Evolutionary Background for Egg Ejection Behaviour and the Role of Motivation for Object Removal

Higher interclutch colour variation can evolve under the pressure of brood parasitism to increase the detection of parasitic eggs. Nest sanitation could be a prerequisite for the evolution of anti-parasite defence in terms of egg ejection. In this respect, we used nest sanitation behaviour as a tool to identify: i) motivation and its underlying function and, ii) which features provoke ejection behaviour. Therefore, we experimentally tested whether size, colour or shape may influence ejection behaviour using artificial flat objects. We found a high interclutch variation in egg colouration and egg size in our tree sparrow (Passer montanus) population. Using colour and size we were in fact able to predict clutch affiliation for each egg. Our experiments further revealed the existence of direct anti-parasite behaviours and birds are able to recognise conspecific eggs, since only experimentally-deposited eggs have been removed. Moreover, experiments with different objects revealed that the motivation of tree sparrows to remove experimental objects from their nests was highest during egg laying for objects of varying size, most likely because of parasitism risk at this breeding stage. In contrary, motivation to remove white objects and objects with edges was higher during incubation stage as behavioural patterns connected to hatching started to emerge. The fact that rejection rate of our flat objects was higher than real egg ejection, suggests that egg ejection in tree sparrows and probably more general in small passerines, to be limited by elevated costs to eject eggs with their beaks. The presence of anti-parasite behaviour supports our suggestion that brood parasitism causes variation in egg features, as we have found that tree sparrows can recognise and reject conspecific eggs in their clutch. In conclusion, in tree sparrows it seems that nest sanitation plays a key role in the evolution of the removal of parasitic eggs.