Telomerase activity can mediate the effects of growth on telomeres during post-natal development in a wild bird.

In wild animals, telomere attrition during early development has been linked with several fitness disadvantages throughout life. Telomerase enzyme can elongate telomeres, but it is generally assumed that its activity is suppressed in most somatic tissues upon birth. However, recent evidence suggests that this may not be the case for long-lived bird species. We have therefore investigated whether telomerase activity is maintained during the postnatal growth period in a wild yellow-legged gull (Larus michahellis) population. Our results indicate that telomerase activity is not negligible in the blood cells, but activity levels sharply decline from hatching to fledging following a similar pattern to the reduction observed in telomere length. Our results further suggest that the observed variation in telomere length may be the result of a negative effect of fast growth on telomerase activity, thus providing a new mechanism through which growth rates may affect telomere dynamics and potentially life-history trajectories.

Postnatal ossification sequences in Acrocephalus scirpaceus and Chroicocephalus ridibundus (Aves: Neognathae): The precocial-altricial spectrum and evolution of compound bones in birds.

Although the development of the avian skeleton has attracted considerable attention, most of the studies have been concentrated on the embryonic period, while studies on the postnatal period are rare. We studied the postnatal development of the skeleton in two phylogenetically distant birds, an altricial passerine Acrocephalus scirpaceus and a semiprecocial charadriiform Chroicocephalus ridibundus. The neonates of the former, despite being altricial, have well-ossified skeleton-the degree of development approaches that of the semiprecocial gull. However, after hatching the limb bones (particularly those of the hind limb) ossify earlier in the gull which is probably related to faster acquisition of locomotor abilities. We have observed that, in contrast to previous reports from neognathous birds, in the ankle of the gull, the ascending process fuses with the astragalus rather than with the calcaneum. This type of development is present in palaeognaths and nonavian dinosaurs but has not yet been reported in neognaths. This indicates a greater diversity within Neognathae and suggests a more complex scenario for the evolution of the avian ankle. However, data from a greater number of species are needed to establish the developmental sequence ancestral for neognathous birds. Furthermore, the sequence of bone fusions in the wrist of Acrocephalus is similar to the fossil-documented evolutionary sequence observed in the phylogeny of early birds, with the semilunate carpal and major metacarpal fusing first, followed by the alular metacarpal fusing with the major metacarpal and then the major and minor metacarpal fusing proximally. These data underscore the importance of developmental studies for reconstructing the evolutionary history.

Effects of drought on the abundance and distribution of non-breeding shorebirds in central California, USA.

Conservation of migratory species requires anticipating the potential impacts of extreme climatic events, such as extreme drought. During drought, reduced habitat availability for shorebirds creates the potential for changes in their abundance and distribution, in part because many species are highly mobile and rely on networks of interior and coastal habitats. Understanding how shorebirds responded to a recent drought cycle that peaked from 2013 to 2015 in central California, USA, will help optimize management of wetlands and fresh water for wildlife. In the Central Valley, a vast interior region that is characterized by a mosaic of wetlands and agricultural lands, we found 22% and 29% decreases in the annual abundance of shorebirds during periods of 3-year drought (2013-2015) and 2-year extreme drought (2014-2015), respectively, when compared to non-drought years. Lower abundance of shorebirds coincided with significant decreases in the mean proportion flooded of survey units (7% and 9%, respectively) that were reliant on fresh water. Drought was associated with lower abundance within both the interior Central Valley and coastal San Francisco Bay for greater and lesser yellowlegs (Tringa melanoleuca and T. flavipes) and long- and short-billed dowitchers (Limnodromus scolopaceus and L. griseus). Only dunlins (Calidris alpina) had patterns of abundance that suggested substantial shifts in distribution between the Central Valley and coastal regions of San Francisco Bay and Point Reyes. Our results indicate that drought has the potential to reduce, at least temporally, shorebird populations and flooded habitat in the Central Valley, and the ability to respond to drought by taking advantage of nearby coastal habitats may limit the long-term effects of drought on some species. Successful conservation strategies must balance the impacts of reduced habitat availability at interior sites with the ability of some migratory shorebirds to adapt rapidly to shifting distributions of resources.

Mercury Uptake Affects the Development of Larus fuscus Chicks.

Current emission and mobilization rates of mercury (Hg) in the environment pose extensive threats to both wildlife and human health. Assessing the exposure risk and effects of Hg contamination in model species such as seabirds is essential to understand Hg risks at the population and ecosystem levels. The lesser black-backed gull (Larus fuscus), a generalist seabird species, is an excellent model species because it forages in both marine and terrestrial habitats, which in turn differ in their Hg exposure risk. To identify possible deleterious effects of Hg exposure on developing L. fuscus chicks, a dietary experiment was carried out and chicks were provided a marine, terrestrial, or mixed diet. The effects of embryonic and dietary Hg exposure on chick body condition and physiological state were assessed at different developmental stages until fledging age (30 d). Overall physiological condition was lower in chicks fed a predominantly marine diet, which coincided with higher Hg loads in blood and primary feathers. However, no effect of dietary uptake of Hg was observed on body condition or in terms of genotoxic damage. Body condition and genotoxic damage correlated instead with Hg exposure during embryonic development, which seems to indicate that embryonic exposure to Hg may result in carry-over effects on later chick development. Environ Toxicol Chem 2020;39:2008-2017. © 2020 SETAC.

Testosterone secretion varies in a sex- and stage-specific manner: Insights on the regulation of competitive traits from a sex-role reversed species.

Testosterone (T) mediates a variety of traits that function in competition for mates, including territorial aggression, ornaments, armaments, and gametogenesis. The link between T and mating competition has been studied mainly in males, but females also face selection pressures to compete for mates. Sex-role reversed species, in which females are the more competitive sex, provide a unique perspective on the role of T in promoting competitive traits. Here, we examine patterns of T secretion in sex-role reversed northern jacanas (Jacana spinosa) during breeding, when females are fertile and males are either seeking copulations or conducting parental care. We measured baseline levels of T in circulation along with a suite of behavioral and morphological traits putatively involved in mating competition. We evaluated hypotheses that levels of T track gonadal sex and parental role, and we begin to investigate whether T and competitive traits co-vary in a sex- and stage- specific manner. Although females had higher expression of competitive traits than males at either breeding stage, we found that females and incubating males had similar levels of T secretion, which were lower than those observed in copulating males. T was correlated with wing spur length in females and testes mass in copulating males, but was otherwise uncorrelated with other competitive traits. These findings suggest that levels of T in circulation alone do not predict variation in competitive traits across levels of analysis, including gonadal sex and parental role. Instead, our findings coupled with prior research indicate that selection for female mating competition and male care may generate different physiological regulation of competitive traits.

Reduced telomere length in embryos exposed to predator cues.

It is often assumed that embryos are isolated from external influences, but recent studies indicate that environmental stressors during prenatal stages can exert long-term negative effects on fitness. A potential mechanism by which predation risk may lastingly shape life-history traits and phenotypes is via effects on telomeres. However, whether prenatal exposure to environmental stressors, such as cues of predator presence, affects postnatal telomere length has not hitherto been investigated. Using an experimental design in which we modified the exposure of yellow-legged gull (Larus michahellis) embryos to social cues of predator presence (i.e. alarm calls), we show that prenatally exposed chicks had shorter telomeres after hatching. As young birds with shorter telomere lengths have reduced fledging success, reproductive success and lifespan, the reduced telomere length in the exposed chicks is likely to have long-term fitness consequences. Moreover, our results provide a mechanistic link through which predators may negatively affect population dynamics.

The Use of Geographic Information Systems for Spatial Ecological Risk Assessments: An Example from the Athabasca Oil Sands Area in Canada.

There is an acknowledged need in ecotoxicology for methods that integrate spatial analyses in risk assessment. This has resulted in the emergence of landscape ecotoxicology, a subdiscipline of ecotoxicology. However, landscape ecotoxicology has yet to become common practice in risk assessment due to the underdevelopment of techniques and a lack of standardized methods. In the present study, we demonstrate how geographic information systems (GISs) can serve as a standardized platform to integrate data, assess spatial patterns of ecotoxicological data for multiple species, and assess relationships between chemical mixture exposures and effects on biota for landscape ecotoxicological risks assessment. We use data collected under the Joint Oil Sands Monitoring Program in the Athabasca Oil Sands Region in Alberta, Canada. This dataset is composed of concentrations of contaminants including metals and polycyclic aromatic compounds, and health endpoints measured in 1100 biological samples, including tree swallows, amphibians, gull and tern eggs, plants, and mammals. We present 3 examples using a GIS as a platform and geospatial analysis to: 1) integrate data and assess spatial patterns of contaminant exposure in the region, 2) assess spatial patterns of exposures to complex mixtures, and 3) examine patterns of exposures and responses across the landscape. We summarize the methods used in the present study into a workflow for ease of use. The GIS methods allow researchers to identify hot spots of contamination, use georeferenced monitoring data to derive quantitative exposure-response relationships, and assess complex exposures with more realism. Environ Toxicol Chem 2019;38:2797-2810. © 2019 SETAC.

The impact of anthropogenic food subsidies on a generalist seabird during nestling growth.

Anthropogenic food subsidies, such as refuse, are an important driver of animal population changes and gulls heavily forage on this food source. Foraging on refuse during the rearing period could affect the acquisition of resources with potential demographic consequences. Using conventional diet analysis and stable isotopes of δ13C and δ15N of blood of Kelp Gull (Larus dominicanus) nestlings, we studied the variation of the chick growth in response to foraging on refuse on a reproductive colony in the Rio de la Plata Estuary in Uruguay. Using Bayesian mixing models on isotopic data, we estimated the proportion and variation of natural food and refuse in the diet of nestlings. Then, we modelled the variation between the mean posterior densities of the food sources and their standard deviation with the nestling morphometric measurements of different sizes. We found that refuse was gradually delivered to Kelp Gull nestlings during the chick rearing period. Additionally, variation of refuse incorporated into nestling tissues increased with nestlings' size. We propose that parents use more isotopically unique food sources during the nestling growth thereby increasing isotopic diversity. This study highlights the need to improve the current waste management system, which is being reviewed in Uruguay. We believe that decision makers should consider the results of this study, which show that refuse is directly impacting coastal ecosystems through mechanisms poorly explored by the environmental sciences.

Temporal and Spatial Distribution of Mercury in Gulls Eggs from the Iberian Peninsula.

We examined how coastal mercury contamination varied spatially and temporally across the Iberian Peninsula by measuring mercury concentrations in the eggs of the sentinel biomonitor yellow-legged gull (Larus michahellis). Samples were collected from eight colonies that ranged from the Atlantic across the south and northern areas of the Mediterranean. We also measured Hg residues in eggs of the one of the most endangered gull species in the world, the Audouin's gull (Larus audouinii) from the Ebro Delta, where colonies of yellow-legged and Audouin's gull co-occur. Fresh eggs were collected in 2009 and 2016 and samples were pooled from each colony for analysis. Mercury concentrations in yellow-legged gulls ranged between 0.4 and 2.8 mg/kg dry weight (dw); although there were no significant differences in concentrations between sampling periods, significant differences were found between colonies. Higher concentrations were associated with northern Mediterranean colonies (Columbretes and Ebro Delta), likely due to proximity to emission sources, circulatory marine currents and diet composition. Mercury concentrations in yellow-legged gull eggs were lower than those reported to result in impaired hatching. Residues in Audouin's gull eggs from the Ebro Delta were significantly higher (4.0-5.6 mg/kg dw) than those in yellow-legged gull from the same location, probably associated with dietary differences. Mercury levels in Audouin's gull were ten times above the benchmark suggested to reduce nest success by 10%. Overall, these results raise concern for adverse health impacts in this protected seabird species and further investigation in Audouin's gull eggs from the Ebro Delta is recommended.

A Video Surveillance System to Monitor Breeding Colonies of Common Terns (Sterna Hirundo).

Many waterbird populations have faced declines over the last century, including the common tern (Sterna hirundo), a waterbird species with a widespread breeding distribution, that has been recently listed as endangered in some habitats of its range. Waterbird monitoring programs exist to track populations through time; however, some of the more intensive approaches require entering colonies and can be disruptive to nesting populations. This paper describes a protocol that utilizes a minimally invasive surveillance system to continuously monitor common tern nesting behavior in typical ground-nesting colonies. The video monitoring system utilizes wireless cameras focused on individual nests as well as over the colony as a whole, and allows for observation without entering the colony. The video system is powered with several 12 V car batteries that are continuously recharged using solar panels. Footage is recorded using a digital video recorder (DVR) connected to a hard drive, which can be replaced when full. The DVR may be placed outside of the colony to reduce disturbance. In this study, 3,624 h of footage recorded over 63 days in weather conditions ranging from 12.8 °C to 35.0 °C produced 3,006 h (83%) of usable behavioral data. The types of data retrieved from the recorded video can vary; we used it to detect external disturbances and measure nesting behavior during incubation. Although the protocol detailed here was designed for ground-nesting waterbirds, the principal system could easily be modified to accommodate alternative scenarios, such as colonial arboreal nesting species, making it widely applicable to a variety of research needs.

Independent and combined effects of egg pro- and anti-oxidants on gull chick phenotype.

Oviparous mothers transfer to their eggs components that have both independent and combined effects on offspring phenotype. The functional interaction between egg components, such as antioxidants and hormones, suggests that a change in the concentration of one component will have effects on offspring traits that depend on the concentration of other interacting components. However, the combined effects of variation in different egg components are virtually unknown. Bird eggs contain vitamin E, a major antioxidant, and also maternal corticosterone. The independent consequences of variation in the egg concentrations of these compounds for offspring phenotype are largely unknown and no study has investigated their combined effects. We manipulated the concentration of vitamin E and corticosterone in the eggs of the yellow-legged gull (Larus michahellis) by administering a physiological (2 s.d.) dose both independently and in combination. We tested for an effect on chick post-natal growth, plasma antioxidant capacity (TAC) and oxidative compounds (TOS). Separate administration of vitamin E or corticosterone caused a reduction in body mass relative to controls, whereas the combined administration of the two compounds reversed their negative effects. These results suggest that maternal egg components, such as antioxidants and steroid hormones, interact and mothers must balance their concentrations in order to achieve optimal offspring phenotype. The functional relationship between vitamin E and corticosterone is corroborated by the observation of positive covariation between these compounds.

First report of a hatched, hand-reared, and released African oystercatcher.

The African oystercatcher Haematopus moquini is a near-threatened wader that is endemic to southern Africa. In the past, the species suffered a drastic decrease in nesting success due to human disturbance. We present the case report of an African oystercatcher that was hatched, hand-reared, and released in the Western Cape, South Africa. African oystercatchers are semi-altricial birds that tend to be highly sensitive to stress; as a result, strategies to minimize stress and the employment of surrogate parents and pre-release acclimatization are important to ensure post-release survival of hand-reared chicks. Considering the lack of literature on the incubation and hand-rearing of oystercatchers, this case report provides a basis for the development of hand-rearing techniques that might be useful for the protection of this and other threatened wader species.

Microbiota of little penguins and short-tailed shearwaters during development.

The establishment and early colonisation of the gastrointestinal (GI) tract has been recognised as a crucial stage in chick development, with pioneering microbial species responsible for influencing the development of the GI tract and influencing host health, fitness and disease status throughout life. Development of the microbiota in long lived seabirds is poorly understood. This study characterised the microbial composition of little penguin and short-tailed shearwater chicks throughout development, using Quantitative Real Time PCR (qPCR) and 16S rRNA sequencing. The results indicated that microbial development differed between the two seabird species with the short-tailed shearwater microbiota being relatively stable throughout development whilst significant fluctuations in the microbial composition and an upward trend in the abundance of Firmicutes and Bacteroidetes were observed in the little penguin. When the microbial composition of adults and chicks was compared, both species showed low similarity in microbial composition, indicating that the adult microbiota may have a negligible influence over the chick's microbiota.

Mercury speciation and subcellular distribution in experimentally dosed and wild birds.

Many bird species are exposed to methylmercury (MeHg) at levels shown to cause sublethal effects. Although MeHg sensitivity and assimilation can vary among species and developmental stages, the underlying reasons (such as MeHg toxicokinetics) are poorly understood. We investigated Hg distribution at the tissue and cellular levels in birds by examining Hg speciation in blood, brain, and liver and Hg subcellular distribution in liver. We used MeHg egg injection of white leghorn chicken (Gallus gallus domesticus), sampled at 3 early developmental stages, and embryonic ring-billed gulls (Larus delawarensis) exposed to maternally deposited MeHg. The percentage of MeHg (relative to total Hg [THg]) in blood, brain, and liver ranged from 94 to 121%, indicating little MeHg demethylation. A liver subcellular partitioning procedure was used to determine how THg was distributed between potentially sensitive and detoxified compartments. The distributions of THg among subcellular fractions were similar among chicken time points, and between embryonic chicken and ring-billed gulls. A greater proportion of THg was associated with metal-sensitive fractions than detoxified fractions. Within the sensitive compartment, THg was found predominately in heat-denatured proteins (∼42-46%), followed by mitochondria (∼15-18%). A low rate of MeHg demethylation and high proportion of THg in metal-sensitive subcellular fractions further indicates that embryonic and hatchling time points are Hg-sensitive developmental stages, although further work is needed across a range of additional species and life stages. Environ Toxicol Chem 2017;36:3289-3298. © 2017 SETAC.

Hippocampal neurogenesis and volume in migrating and wintering semipalmated sandpipers (Calidris pusilla).

Long distance migratory birds find their way by sensing and integrating information from a large number of cues in their environment. These cues are essential to navigate over thousands of kilometers and reach the same breeding, stopover, and wintering sites every year. The semipalmated sandpiper (Calidris pusilla) is a long-distance migrant that breeds in the arctic tundra of Canada and Alaska and winters on the northeast coast of South America. Its fall migration includes a 5,300-kilometer nonstop flight over the Atlantic Ocean. The avian hippocampus has been proposed to play a central role in the integration of multisensory spatial information for navigation. Hippocampal neurogenesis may contribute to hippocampal function and a variety of factors including cognitive activity, exercise, enrichment, diet and stress influence neurogenesis in the hippocampus. We quantified hippocampal neurogenesis and volume in adult migrating and wintering semipalmated sandpipers using stereological counts of doublecortin (DCX) immunolabeled immature neurons. We found that birds captured in the coastal region of Bragança, Brazil during the wintering period had more DCX positive neurons and larger volume in the hippocampus than individuals captured in the Bay of Fundy, Canada during fall migration. We also estimate the number of NeuN immunolabeled cells in migrating and wintering birds and found no significant differences between them. These findings suggest that, at this time window, neurogenesis just replaced neurons that might be lost during the transatlantic flight. Our findings also show that in active fall migrating birds, a lower level of adult hippocampal neurogenesis is associated with a smaller hippocampal formation. High levels of adult hippocampal neurogenesis and a larger hippocampal formation found in wintering birds may be late occurring effects of long distance migratory flight or the result of conditions the birds experienced while wintering.

Effects of developmental conditions on growth, stress and telomeres in black-legged kittiwake chicks.

Early-life conditions can drive ageing patterns and life history strategies throughout the lifespan. Certain social, genetic and nutritional developmental conditions are more likely to produce high-quality offspring: those with good likelihood of recruitment and productivity. Here, we call such conditions "favoured states" and explore their relationship with physiological variables during development in a long-lived seabird, the black-legged kittiwake (Rissa tridactyla). Two favoured states were experimentally generated by manipulation of food availability and brood size, while hatching order and sex were also explored as naturally generating favoured states. Thus, the favoured states we explored were high food availability, lower levels of sibling competition, hatching first and male sex. We tested the effects of favoured developmental conditions on growth, stress, telomere length (a molecular marker associated with lifespan) and nestling survival. Generation of favoured states through manipulation of both the nutritional and social environments furthered our understanding of their relative contributions to development and phenotype: increased food availability led to larger body size, reduced stress and higher antioxidant status, while lower sibling competition (social environment) led to lower telomere loss and longer telomere lengths in fledglings. Telomere length predicted nestling survival, and wing growth was also positively correlated with telomere length, supporting the idea that telomeres may indicate individual quality, mediated by favoured states.

Variation in Growth Drives the Duration of Parental Care: A Test of Ydenberg's Model.

The duration of parental care in animals varies widely, from none to lifelong. Such variation is typically thought to represent a trade-off between growth and safety. Seabirds show wide variation in the age at which offspring leave the nest, making them ideal to test the idea that a trade-off between high energy gain at sea and high safety at the nest drives variation in departure age (Ydenberg's model). To directly test the model assumptions, we attached time-depth recorders to murre parents (fathers [which do all parental care at sea] and mothers; [Formula: see text] of each). Except for the initial mortality experienced by chicks departing from the colony, the mortality rate at sea was similar to the mortality rate at the colony. However, energy gained by the chick per day was ∼2.1 times as high at sea compared with at the colony because the father spent more time foraging, since he no longer needed to spend time commuting to and from the colony. Compared with the mother, the father spent ∼2.6 times as much time diving per day and dived in lower-quality foraging patches. We provide a simple model for optimal departure date based on only (1) the difference in growth rate at sea relative to the colony and (2) the assumption that transition mortality from one life-history stage to the other is size dependent. Apparently, large variation in the duration of parental care can arise simply as a result of variation in energy gain without any trade-off with safety.

Mercury exposure may influence fluctuating asymmetry in waterbirds.

Variation in avian bilateral symmetry can be an indicator of developmental instability in response to a variety of stressors, including environmental contaminants. The authors used composite measures of fluctuating asymmetry to examine the influence of mercury concentrations in 2 tissues on fluctuating asymmetry within 4 waterbird species. Fluctuating asymmetry increased with mercury concentrations in whole blood and breast feathers of Forster's terns (Sterna forsteri), a species with elevated mercury concentrations. Specifically, fluctuating asymmetry in rectrix feather 1 was the most strongly correlated structural variable of those tested (wing chord, tarsus, primary feather 10, rectrix feather 6) with mercury concentrations in Forster's terns. However, for American avocets (Recurvirostra americana), black-necked stilts (Himantopus mexicanus), and Caspian terns (Hydroprogne caspia), the authors found no relationship between fluctuating asymmetry and either whole-blood or breast feather mercury concentrations, even though these species had moderate to elevated mercury exposure. The results indicate that mercury contamination may act as an environmental stressor during development and feather growth and contribute to fluctuating asymmetry of some species of highly contaminated waterbirds. Environ Toxicol Chem 2017;36:1599-1605. Published 2016 Wiley Periodicals Inc. on behalf of SETAC. This article is a US government work and, as such, is in the public domain in the United States of America.

How Do Growth and Sibling Competition Affect Telomere Dynamics in the First Month of Life of Long-Lived Seabird?

Telomeres are nucleotide sequences located at the ends of chromosomes that promote genome stability. Changes in telomere length (dynamics) are related to fitness or life expectancy, and telomere dynamics during the development phase are likely to be affected by growth and stress factors. Here, we examined telomere dynamics of black-tailed gull chicks (Larus crassirostris) in nests with and without siblings. We found that the initial telomere lengths of singletons at hatching were longer than those of siblings, indicating that singletons are higher-quality chicks than siblings in terms of telomere length. Other factors likely affecting individual quality (i.e., sex, laying date, laying order of eggs, and clutch size) were not related to telomere lengths. Within broods, initial telomere lengths were longer in older chicks than in younger chicks, suggesting that maternal effects, which vary with laying sequence, influence the initial lengths. Additionally, telomeres of chicks with a sibling showed more attrition between hatching and fledging than those of singleton chicks, suggesting that being raised with siblings can cause a sustained competitive environment that leads to telomere loss. High growth rates were associated with a low degree of telomere shortening observed in older siblings, perhaps because slower growth reflects higher food stress and/or higher aerobic metabolism from increased begging effort. Our results show that developmental telomere attrition was an inevitable consequence in two-chick nests in the pre- and post-hatching microenvironments due to the combination of social stress within the nest and maternal effects. The results of our study shed light on telomere dynamics in early life, which may represent an important physiological undercurrent of life-history traits.

Timing of Breeding Determines Growth and Development in a Long-Distance Migratory Bird.

The timing of breeding can have significant consequences for adult and offspring fitness, yet our current hypotheses of seasonal timing focus on the parent perspective. When offspring survival is affected by timing of breeding, we expect to see offspring mechanisms to detect and respond to cues of seasonal timing. Avian embryos respond to photoperiod and seasonal cues during development and in this study we evaluate the influence of photoperiod and season on posthatching growth and development in Franklin's gull (Leucophaeus pipixcan). Early- and late-season chicks exposed to short and long photoperiods during development were reared under common garden conditions. Photoperiod had no effect on posthatching growth and development, but seasonal effects present in the egg (maternal egg effects or genetic) did influence posthatching growth and development. Late-season chicks grew body mass and primary flight feathers at faster rates than early-season chicks, which we hypothesize facilitates independence and readiness for migration. Growth rates are complex phenotypes and we propose a general growth model that incorporates delays in negative feedback systems regulating growth. We show that the timing of breeding programs intrinsic growth rates in offspring, which suggests that many of the metrics used to describe seasonal patterns of reproductive success may be biased.