Subadult Life Stages Research Articles

Long‐term tracking captures the timing of ontogenetic niche shifts in northeast Pacific white sharks

AbstractOntogenetic changes in area use, habitat use, and trophic interactions play an important role in the ecology, demography, and ultimately population dynamics of many species. Assumed to be driven by shifting life‐history requirements, trophic niche shifts in white sharks (Carcharodon carcharias) are well documented, but the timing of the spatial niche shift that is hypothesized to occur with the trophic niche shift remains poorly understood. To document how fine‐scale area use varies as sharks age and the timing of the ontogenetic spatial shift of this top predator, we tracked individual white sharks tagged as young‐of‐the‐year or young juveniles over multiple years. Using data from juvenile white sharks detected over multiple years in a nursery habitat with a high‐density receiver array, we found no difference in area use with age. However, using a coast‐wide receiver array including nursery and adult habitat, we found the probability of detecting a juvenile white shark in nursery habitat decreased with age, with a concurrent increasing probability of detection in adult habitat. As the conservation and management of this species relies on understanding nursery habitat use and age‐related movements, data presented here address an important knowledge gap for the understudied juvenile to subadult life stages and the ontogenetic habitat shift of this species.

Toxicokinetic Models for Bioconcentration of Organic Contaminants in Two Life Stages of White Sturgeon (Acipenser transmontanus).

The white sturgeon (Acipenser transmontanus) is an endangered ancient fish species that is known to be particularly sensitive to certain environmental contaminants, partly because of the uptake and subsequent toxicity of lipophilic pollutants prone to bioconcentration as a result of their high lipid content. To better understand the bioconcentration of organic contaminants in this species, toxicokinetic (TK) models were developed for the embryo-larval and subadult life stages. The embryo-larval model was designed as a one-compartment model and validated using whole-body measurements of benzo[a]pyrene (B[a]P) metabolites from a waterborne exposure to B[a]P. A physiologically based TK (PBTK) model was used for the subadult model. The predictive power of the subadult model was validated with an experimental data set of four chemicals. Results showed that the TK models could accurately predict the bioconcentration of organic contaminants for both life stages of white sturgeon within 1 order of magnitude of measured values. These models provide a tool to better understand the impact of environmental contaminants on the health and the survival of endangered white sturgeon populations.

Temperature and food sources influence subadult development and blood-feeding response of Culicoides obsoletus (sensu lato) under laboratory conditions

BackgroundCulicoides obsoletus (s.l.) is the most abundant Culicoides species in northern Europe and an important vector of bluetongue virus and Schmallenberg virus. Nevertheless, information on its subadult life stages remains scarce and no laboratory-reared colony exists.MethodsC. obsoletus (s.l.) adults were collected in Belgium and transferred to the laboratory in an attempt to establish a laboratory-reared colony. C. obsoletus (s.l.) were reared from eggs to adults at different temperatures (28 °C, 24 °C, 20/16 °C) and under different food regimes.ResultsThe most suitable temperature for rearing seemed to be 24 °C for most developmental parameters, but resulted in a biased 3:1 male/female sex ratio. The latter could be optimized to a 1:1 sex ratio when a 20/16 °C day/night temperature gradient was applied, but rearing at these low temperature conditions resulted in significantly lower egg hatching and pupation rates and a longer subadult development time. Independent of the rearing temperature, adding dung as an additional food source during larval development resulted in a significantly higher adult emergence rate and a decrease in subadult development time. Furthermore, blood-feeding rates of field-collected C. obsoletus (s.l.) were compared for different blood sources and feeding systems. The overall blood-feeding success was low and only successful with cotton pledgets (2.7% blood-fed midges) and through a membrane system with chicken skin (3.5% blood-fed midges). Higher feeding rates were obtained on cattle blood compared to sheep blood.ConclusionsThese results will help us to determine the necessary conditions to rear a viable laboratory colony of this important vector species, although further optimization is still required.Graphical abstract

Alveolar Trough: Formalizing an Arcus Alveolaris Analog in a Sauropsid Model

Mammals and crocodylians share thecodont tooth implantation, wherein bony sockets (alveoli) enclose tooth roots. Mammalian alveoli are composed of a thin layer of remodeled haversian bone forming the socket, and cancellous bone filling the space between the socket and the jaw elements, together forming an arcus alveolaris. The sockets act as an anchoring attachment for the periodontal ligament and support the dentition, and recent research has shown that alveoli have a role in tooth formation. Complexity in mammal heterodonty depends, in part, on alveoli mechanically constraining the developing crown: high alveolar constraint produces more complex crowns. Previously, we have shown a significant relationship between alveolar and dental crown morphologies in Alligator mississippiensis: as each new tooth contributes tissue to the socket wall, the alveoli limit shape variation of subsequent crown generations. In yearling caimans, alveolar bone type is identified as lamellar bundle bone; however, there is to-date no complete morphological description of the alveolar anatomy of crocodylians. In this study, we describe the unique alveolar anatomy in extant crocodylians and evaluate the need for specific anatomical terminology based on deviations from the mammalian standard. From micro-computed tomography (μCT) data, we digitally reconstructed the jaws of embryonic, hatchling, juvenile, and subadult life stages of Alligator, parsing alveolar bone from other jaw elements. We compared these μCT datasets with those of model rodent species (Microtus, Rattus, Napaeozapus) and to the dental literature. Our results show alligators lack the mammalian-type arcus alveolus. Instead, they have a thick trough of lamellar bundle bone connected to adjacent jaw elements by thin osseous struts and direct fusion on buccal and lingual contacts. Notably, cancellous bone is absent. The trough is retained throughout ontogeny and is the foundation onto which interdental septa are added. Both trough and septa thicken with age as replacement-tooth size increases. Current anatomical terminology for alveoli fits the integrated mammalian jaw type well, but the crocodylian type is markedly different. The crocodylian alveolar condition is principally composed of a thickened trough of lamellar bundle bone, indicating a need for sauropsid-specific terminology to reflect this analogous configuration. The term alveolar trough is suggested as it has been used previously to describe alveolar features in fossil reptiles but lacks a formal definition, which we now erect. Alveus alveolaris (L., “alveolar trough”)—a thick channel of lamellar bundle bone in the jaws of, for example, crocodylians that provides the surface for gomphotic thecodonty and connects to jaw elements through direct fusion, but without cancellous bone. The delineation of the alveolar trough has far-reaching implications to dental form and function. Primarily, it calls attention to this apparently unique feature of crocodylian jaws, which should inform future research directions to more discretely address its development, function, and evolution. In addition, the trough—alongside interdental septa and rootedness—may help to clarify the role of tooth socket configurations as potential key innovations in tetrapod dental evolution.

Estimating the survival of unobservable life stages for a declining frog with a complex life history

AbstractDemographic models enhance understanding of drivers of population growth and inform conservation efforts to prevent population declines and extinction. For species with complex life histories, however, parameterizing demographic models is challenging because some life stages can be difficult to study directly. Integrated population models (IPMs) empower researchers to estimate vital rates for organisms that have cryptic or widely dispersing early life stages by integrating multiple demographic data sources. For a stream‐inhabiting frog (Rana boylii) that is declining through much of its range in Oregon and California, USA, we collected egg‐mass counts and capture–mark–recapture data on adults from two populations in California to fit IPMs that estimate adult abundance and the survival rate of both marked and unobserved life stages. Estimates of adult abundance based on long‐term monitoring of egg‐mass counts showed that study populations fluctuated greatly inter‐annually but were stable at longer timescales (i.e., decades). Adult female survival during 5–6 yr of capture–mark–recapture study periods was nearly equal in each population. Survival rate of R. boylii eggs to the subadult stage is low on average (0.002) but highly variable among years depending on post‐oviposition stream flow. Population viability analysis showed that survival of adult and subadult life stages has the greatest proportional effect on population growth; the survival of egg and tadpole life stages, however, is more malleable by management interventions. For example, simulations showed head‐starting of tadpoles, salvaging stranded egg masses, and limiting aseasonal pulsed flows could dramatically reduce the threat of extirpation. This study demonstrates the value of integrating multiple demographic data sources to construct models of population dynamics in species with complex life histories.

Evaluation of a Deepwater Release Method for Hatchery‐Reared Lake Sturgeon

AbstractHatchery rearing and stocking of young Lake Sturgeon Acipenser fulvescens have become key management and species recovery tools in many jurisdictions, yet there has been relatively little investigation into the optimization of release methods. Based on the contemporary understanding of the species’ ecology in Boreal Shield rivers, it was hypothesized that poststocking survival and/or within‐reach retention could be improved via release of hatchery‐reared fish directly into the deepwater habitats that are preferred by juvenile and subadult life stages. Acoustic telemetry and mark–recapture methods were used to evaluate this hypothesis. In total, 390 PIT‐tagged age‐1 Lake Sturgeon (mean ± SD of length measured 1 week prior to stocking = 242 ± 29 mm FL) were released during spring 2015 from shore at the base of a set of falls on the Nelson River, Manitoba (mimicking the status quo stocking procedure for the reach), and 391 PIT‐tagged individuals (240 ± 27 mm FL) were released approximately 4.2 river kilometers downstream of the shore release location into an approximately 750‐m‐long patch of deepwater habitat (maximum depth = 15 m) using the deepwater release method. Of the released fish, 30 (15 per stocking method) were implanted with acoustic transmitters. In total, 23% and 22% of the stocked fish were recaptured in gill‐net surveys conducted during fall 2015 and 2016, respectively. Recapture proportions associated with the two release types were not significantly different. Acoustic telemetry revealed considerable variation among individuals and offered general insight into poststocking behavior but provided no direct support for the primary hypothesis. Despite the null results of the current study, optimization of release methods for Lake Sturgeon may warrant further investigation.

A Covered Cod-End and Tow-Path Evaluation of Midwater Trawl Gear Efficiency for Catching Delta Smelt (Hypomesus transpacificus)

Author(s): Mitchell, Lara; Newman, Ken; Baxter, Randall | Abstract: For nearly 50 years, the California Department of Fish and Wildlife has used a midwater trawl to intensively monitor fish populations in the San Francisco Estuary during the fall, sampling over 100 locations each month. The data collected have been useful for calculating indices of fish abundance and for detecting and documenting the decline of the endangered fish species delta smelt (Hypomesus transpacificus). However, efforts to calculate estimates of absolute abundance have been hampered by the lack of information on gear efficiency, in particular questions about contact selectivity and the effect of tow method on catches. To answer these questions we conducted a study that used a covered cod end on a net towed either near the surface, referred to as a surface tow, or throughout the water column, referred to as an oblique tow. A contact selectivity model was fit to estimate the probability that a delta smelt that has come into contact with the net is retained in the cod end of the net conditional on its body length. Full retention of delta smelt was found to occur around 60 mm fork length. Delta smelt catch densities for the surface tows were an order of magnitude greater than densities in the oblique tows, suggesting a surface orientation at the sub-adult life stage. These results represent an important step in being able to calculate absolute abundance estimates of the delta smelt population size using decades’ worth of monitoring data.

Using fisheries modeling to assess candidate species for marine fisheries enhancement

Selecting target species or stocks in which releases of hatchery fish can contribute effectively to fisheries management goals is a key challenge in many fisheries enhancement programs. Here we show how fisheries modeling informed by stock assessments can be used to evaluate contributions of stocked fish to fisheries and how these contributions are influenced by life history and fishery attributes including regulatory policies and angler effort. We built an age-structured population model to quantitatively assess enhancement contributions to multiple fisheries management objectives: predicted catch, predicted harvest, abundance of catchable fish, abundance of harvestable fish and total spawning biomass. We used this model to evaluate candidate species for marine fisheries enhancement in Florida, where hatchery production capacity is scheduled to expand over the next decade yet it is unclear how fisheries managers can best use this capacity to achieve management objectives. We evaluated five candidate marine fishes in Florida: red drum Sciaenops ocellatus, spotted seatrout Cynoscion nebulosus, common snook Centropomus undecimalis, southern flounder Paralichthys lethostigma and red snapper Lutjanus campechanus. Comparative analysis shows that contribution of released fish to fisheries outcomes tend to decline with increasing time between release and capture or harvest. Enhancement of red drum, a species targeted by anglers during sub-adult life stages, is predicted to yield lower numbers of stocked fish entering the recruited population compared to alternative species but to contribute more to catch and harvest objectives. Our results demonstrate how commonly available biological information can be integrated with quantitative modeling approaches to provide useful information to managers tasked with identifying best uses of increasing enhancement capacity.

Diet Analysis of Subadult Kemp’s Ridley (Lepidochelys kempii) Turtles from West-Central Florida

Abstract The present study is the first to characterize Kemp’s ridley turtle (Lepidochelys kempii) diets between the west-central Florida estuaries of Tampa Bay to Charlotte Harbor. We analyzed the stomach contents of 20 stranded subadult L. kempii and found that their diets were primarily carnivorous, consisting mostly of calico crab (Hepatus epheliticus), stone crab (Menippe mercenaria), and blue crab (Callinectes sapidus). In addition, we found uncommon prey items including fish and horseshoe crab (Limulus polyphemus), suggesting these L. kempii are opportunistic feeders. When separated into 2 size classes (25–45 [n = 9] and > 45 [n = 11] cm straight carapace length), there was a significant difference in the turtles’ diet composition. These new insights into the ecology and life history of a critically endangered sea turtle reveal essential prey resources used by a poorly studied yet crucial subadult life stage.

Behaviour and mimicry in the juvenile and subadult life stages of the mesopelagic squid Chiroteuthis calyx

Cephalopods are common inhabitants of the deep ocean's mesopelagic zones worldwide, yet very little is known about their behaviour due to the inaccessibility of this environment. Recent studies suggest that, contrary to historical predictions, deep-sea cephalopods exhibit a wide array of visual behaviours. We used in situ footage from remotely operated vehicles, coupled with laboratory observations to assemble the first behavioural ethogram for the juvenile and subadult life stages of the mesopelagic squid, Chiroteuthis calyx. The number of behavioural components we described is comparable to or exceeds those recognized in ethograms of shallow-water teuthids. We used the ethogram to make a detailed behavioural comparison between the juvenile and subadult life stages, and found distinctly different patterns. Behavioural and morphological differences between the two life stages support the hypothesis that juvenile C. calyx mimic the abundant siphonophore Nanomia bijuga, in order to deter predation.

Influence of size on the sources of energy consumed by overwintering walleye pollock ( Theragra chalcogramma)

The critical size hypothesis proposes the risks of winter mortality are greatest for small individuals in fish populations. This results from size-dependent predation and starvation of wintering fishes. We extend this idea to walleye pollock ( Theragra chalcogramma) and argue size-dependence leads to different wintering strategies among subadult life stages. We sampled fish quarterly, measured their size, growth and energy allocation. By comparing the contributions of endogenous energy sources (storage and structure) to metabolic demand in young-of-the-year (YOY) and juvenile pollock over winter we determined how length influenced their winter foraging requirement. From this we inferred the relative risks of starvation and predation for different sized fish. Young-of-the-year (≤ 170 mm) experienced high starvation risk and relied on foraging to meet routine metabolic cost. Consequently, they consumed relatively little storage or structural energy over winter. In contrast, juveniles (> 170 mm and ≤ 270 mm) responded to the risk of predation by consuming significant amounts of protein and structural lipids while minimizing foraging. Consistent with these observations we found YOY maximized growth in fall while juveniles maximized energy storage. In spring, YOY resumed growth earlier than juveniles. These data indicate the critical size and period hypothesis can be extended to walleye pollock.

Genetic and ecological impacts of heavy metal and flooding stress on the earthworm Lumbricus rubellus in floodplains of the Rhine river

In the highly polluted river Rhine system, earthworms face environmental stress resulting from flooding and elevated heavy metal concentrations in the floodplain soil. Previous field studies have revealed adaptation to flooding for the earthworm species Lumbricus rubellus as this species matures at a lower weight in floodplain sites with a high frequency of flooding compared to less frequently flooded sites. Also heavy metals have effects on L. rubellus and heavy metals are influencing the genetic composition of this species. In this study, it was tested whether flooding and heavy metals had an impact on the genetic composition of L. rubellus living in floodplains along the river Rhine system. Earthworms were sampled at three sites previously studied along the river to assess earthworm diversity, biomass, density, and individual weight, and developmental status of L. rubellus. The genetic variation by means of isozymes was studied for 175 individuals. The results showed lowest density of L. rubellus adult and sub-adult life-stages and lowest individual weight of these life-stages at the frequent inundated site. The genetic composition, however, showed no effects of flooding on the genetic composition, but effects of heavy metals could not be ruled out.

Habitat disturbances differentially affect individual growth rates in a long‐lived turtle

AbstractDisturbances often help structure ecological communities, and their impacts may have consequences on population dynamics and long‐term species persistence. Should disturbances affect resources, a trade‐off may result between reproduction and individual growth, which in turn could affect the timing of sexual maturity in animals dependent on reaching a requisite size for the onset of maturation. We used a 14‐year mark–recapture dataset to determine the effects of catastrophic storms and the removal of nonindigenous vegetation on individual growth rates of a long‐lived turtle Terrapene carolina bauri. Adult male growth rates increased 19% after the disturbances, whereas female growth rates decreased by a similar percentage. Juvenile growth rates briefly increased, but as these animals became subadults, their growth rates slowed after disturbance, a change more pronounced in females than males. After the disturbances, the onset of male sexual maturity decreased by c. 1 years (from 10.8 to 9.5 years), female maturity was delayed by 2.5 years (from 8.5 to 11.0 years), and the subadult life stage was extended from 2 to 3.5 years. With resources and habitats similarly available to adults, we hypothesize that adult females diverted resources from growth to reproduction, whereas males allocated available resources to growth. Subadult growth rates decreased regardless of sex, implying that fewer or lower quality prey were available to smaller sized turtles in the years following disturbance. The results of this study suggest that habitat disturbances affected individual growth rates differently according to sex and life stage, which in turn affected the timing of maturation. In long‐lived vertebrates, such perturbations on life‐history traits such as growth rates likely affect population recovery, and may help to explain why turtle populations recover slowly following catastrophic disturbance, even when adult survivability is high.

Terrestrial Movements and Microhabitat Selection of Overwintering Subadult Eastern Mud Turtles (Kinosternon Subrubrum) in Southwest Georgia

Abstract Although there is increasing recognition of the importance of terrestrial habitat to aquatic fauna, little is known about the specific habitat requirements of these species at a fine scale within the terrestrial landscape. Our knowledge of subadult life stages of many species, specifically aquatic turtles, is particularly depauperate. We used radio-telemetry to determine the timing and extent of terrestrial movements of 11 subadult Eastern Mud Turtles, Kinosternon subrubrum, during the winter. We also quantified microhabitat variables (ground cover composition, shrub cover, and canopy cover) of temporary refugia and overwintering sites (hibernacula) of radio-tagged turtles. On average, hibernacula sites were 72 m from the wetland (defined as the water's edge). Turtles remained at hibernacula a mean of 107 days before emerging in the spring. Radio-tagged turtles selected winter hibernacula with a large component of leaf and pine litter and less tree cover than temporary refugia. The leaf litter ma...

Do Penaeid Shrimps have a Preference for Mangrove Habitats? Distribution Pattern Analysis on Inhaca Island, Mozambique

Scientific information on how penaeid shrimps are distributed within mangrove ecosystems is scarce, which presents an obstacle for fisheries as well as mangrove management. This study investigated the prime nursery microhabitats for the two major commercial species in Mozambique—Penaeus indicus and Metapenaeus monoceros. Stake net enclosures were used to sample shrimps living among unvegetated shallows and mangroves at Inhaca Island, Mozambique, during three consecutive spring tide periods. Four microhabitats were sampled: (1) sand flat; (2) fringe Avicennia marina on sandy substrate; (3) fringe A. marina on muddy substrate; and (4) interior A. marina adjacent to the supratidal terrestrial margin.P. indicus had a significant preference for fringe mangroves over the adjacent sand flat (P<0·001 and P=0·05). Postlarval shrimps only occupied the sand flat, whereas the mangrove was utilized by postlarval, juvenile and sub-adult life stages. Within the fringe mangrove, there was no correlation between shrimp abundance and organic content of sediment (5·7–11·6 shrimpsm−2). Shrimps utilized the most interior margin of the mangroves (0·35 shrimpsm−2), although catch rates were significantly lower than in the mangrove fringe (P<0·001). M. monoceros was significantly (P<0·01), more abundant in the sand flat (0·44–2·1 shrimpsm−2) than in the mangrove fringe (0·04–0·61 shrimpsm−2), although this habitat preference was not evident for juvenile and sub-adult life stages.The results demonstrate the extensive use of mangrove habitats by penaeid shrimps. The confinement to mangroves for P. indicus, but not for M. monoceros, is discussed in the context of habitat characteristics and predation avoidance behaviour. Methodological considerations of the stake net technique are also outlined.