Temperature preference of juvenile lumpfish (Cyclopterus lumpus) originating from the southern and northern parts of Norway

Fish are ectothermic animals and have body temperatures close to that of the water they inhabit. They can still control their body temperatures by selecting habitats with temperatures that maximize their growth, feed conversion and wellbeing. Lumpfish, Cyclopterus lumpus, is widely distributed in the North Atlantic Ocean and therefore exposed to variable water temperatures. Lumpfish is extensively used as cleanerfish in salmon farming in Norway and exposed to a wide temperature range along the north-south axis of the Norwegian coastline. But, if these temperature ranges correspond to the preference temperatures of lumpfish is not known. If lumpfish has adapted to regional temperatures along the Norwegian coast, differences in preference temperature for fish from different regions should be evident. In a selective breeding perspective, different selection lines for preference temperature would then be useful for further development of lumpfish as a cleanerfish.We subjected lumpfish juveniles weighing 154–426g originated from northern (Group North – GN) and southern (Group South – GS) Norway to a temperature preference test, using an electronic shuttle box system. The system allowed the fish to control the water temperature by moving between two chambers, and thereby choosing its preferred temperature in the range from 5 to 16 °C. We started the temperature at 7.8 ± 1.37 °C for GN and 7.58 ± 1.34 °C for GS, but all the fish except four (two each from GN and GS) chose lower temperatures (5.03–7.6 °C) in the first 18 h and stayed closer to that temperature during the next 30 h. Based on the results, GN and GS lumpfish preferred 6.92 ± 1.8 and 6.2 ± 1.2, respectively, and there was no significant difference between the groups. Neither was there any significant difference in growth rates (SGR) between the two groups. Based on our results, we suggest that lumpfish from any geographical origin along the Norwegian coast can be used anywhere in Norway. It follows that lumpfish from a single selection line could be used at any salmon farm in Norway independent of its location.     

Short-term movements of larval and juvenile lumpfish, Cyclopterus lumpus L., in tidepools

Larval and juvenile lumpfish, Cyclopterm lumpus L., which attach to marine algae and eelgrass using a ventral sucker, were marked and recaptured in a series of experiments along Schoodic Peninsula, Maine, U.S.A. A repeat-marking experiment in 1988 indicated immigration and, possibly, emigration in tidepools. Yet, some individuals remained in the same tidepool for up to 25 days. Experiments with marked groups of fish in 1988 and 1989 revealed significant short-term residence of individual lumpfish; up to 79% of marked fish were recaptured in the same tidepool 2 days later, even after major storms. A translocated group of 34 lumpfish left the new tidepool within 1 day, but two individuals returned to the home tidepool within 6 days. Extended inhabitance of tidepools by larval and juvenile lumpfish seems to be a function of availability of food and algal cover.     

locuseater and shadowboxer: programs to optimize experimental design and multiplexing strategies for genetic mark–recapture

Genetic mark–recapture requires efficient methods of uniquely identifying individuals. ‘Shadows’ (individuals with the same genotype at the selected loci) become more likely with increasing sample size, and bias harvest rate estimates. Finding loci is costly, but better loci reduce analysis costs and improve power. Optimal microsatellite panels minimize shadows, but panel design is a complex optimization process. locuseater and shadowboxer permit power and cost analysis of this process and automate some aspects, by simulating the entire experiment from panel design to harvest rate estimation.     

dropout: a program to identify problem loci and samples for noninvasive genetic samples in a capture‐mark‐recapture framework

Abstract Genotyping error, often associated with low‐quantity/quality DNA samples, is an important issue when using genetic tags to estimate abundance using capture‐mark‐recapture (CMR). dropout , an MS‐Windows program, identifies both loci and samples that likely contain errors affecting CMR estimates. dropout uses a ‘bimodal test’, that enumerates the number of loci different between each pair of samples, and a ‘difference in capture history test’ (DCH) to determine those loci producing the most errors. Importantly, the DCH test allows one to determine that a data set is error‐free. dropout has been evaluated in McKelvey & Schwartz (2004) and is now available online.     

Complete tag loss in capture–recapture studies affects abundance estimates: An elephant seal case study

1. In capture–recapture studies, recycled individuals occur when individuals lose all of their tags and are recaptured as though they were new individuals. Typically, the effect of these recycled individuals is assumed negligible.
2. Through a simulation‐based study of double‐tagging experiments, we examined the effect of recycled individuals on parameter estimates in the Jolly–Seber model with tag loss (Cowen & Schwarz, 2006). We validated the simulation framework using long‐term census data of elephant seals.
3. Including recycled individuals did not affect estimates of capture, survival, and tag‐retention probabilities. However, with low tag‐retention rates, high capture rates, and high survival rates, recycled individuals produced overestimates of population size. For the elephant seal case study, we found population size estimates to be between 8% and 53% larger when recycled individuals were ignored.
4. Ignoring the effects of recycled individuals can cause large biases in population size estimates. These results are particularly noticeable in longer studies.

     

Genetic fingerprinting proves cross‐correlated automatic photo‐identification of individuals as highly efficient in large capture–mark–recapture studies

Capture–mark–recapture (CMR) approaches are the backbone of many studies in population ecology to gain insight on the life cycle, migration, habitat use, and demography of target species. The reliable and repeatable recognition of an individual throughout its lifetime is the basic requirement of a CMR study. Although invasive techniques are available to mark individuals permanently, noninvasive methods for individual recognition mainly rest on photographic identification of external body markings, which are unique at the individual level. The re‐identification of an individual based on comparing shape patterns of photographs by eye is commonly used. Automated processes for photographic re‐identification have been recently established, but their performance in large datasets (i.e., > 1000 individuals) has rarely been tested thoroughly. Here, we evaluated the performance of the program AMPHIDENT, an automatic algorithm to identify individuals on the basis of ventral spot patterns in the great crested newt (Triturus cristatus) versus the genotypic fingerprint of individuals based on highly polymorphic microsatellite loci using GENECAP. Between 2008 and 2010, we captured, sampled and photographed adult newts and calculated for 1648 samples/photographs recapture rates for both approaches. Recapture rates differed slightly with 8.34% for GENECAP and 9.83% for AMPHIDENT. With an estimated rate of 2% false rejections (FRR) and 0.00% false acceptances (FAR), AMPHIDENT proved to be a highly reliable algorithm for CMR studies of large datasets. We conclude that the application of automatic recognition software of individual photographs can be a rather powerful and reliable tool in noninvasive CMR studies for a large number of individuals. Because the cross‐correlation of standardized shape patterns is generally applicable to any pattern that provides enough information, this algorithm is capable of becoming a single application with broad use in CMR studies for many species.     

Long‐term mark‐and‐recapture study of a freshwater mussel reveals patterns of habitat use and an association between survival and river discharge

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Assessing the abundance of Bristol Bay belugas with genetic mark‐recapture methods

The Bristol Bay stock of beluga whales (Delphinapterus leucas) is genetically distinct and resides in Bristol Bay year‐round. We estimated the abundance of this population using genetic mark‐recapture, whereby genetic markers from skin biopsies, collected between 2002 and 2011, were used to identify individuals. We identified 516 individual belugas in two inner bays, 468 from Kvichak Bay and 48 from Nushagak Bay, and recaptured 75 belugas in separate years. Using a POPAN Jolly‐Seber model, abundance was estimated at 1,928 belugas (95% CI = 1,611–2,337), not including calves, which were not sampled. Most belugas were sampled in Kvichak Bay at a time when belugas are also known to occur in Nushagak Bay. The pattern of genetic recaptures and data from belugas with satellite transmitters suggested that belugas in the two bays regularly mix. Hence, the estimate of abundance likely applies to all belugas within Bristol Bay. Simulations suggested that POPAN estimates of abundance are robust to most forms of emigration, but that emigration causes negative bias in both capture and survival probabilities. Because it is likely that some belugas do not enter the sampling area during sampling, our estimate of abundance is best considered a minimum population size.     

Walking with worms: coral‐associated epifaunal nematodes

Aims To study the community structure and habitat preferences of the Epsilonematidae and Draconematidae in coral degradation zones. To assess the contribution of different localities and microhabitats to meiobenthic diversity in such ecosystems. To discuss dispersive capacities and the occurrence of cryptic species in meiobenthic organisms. Location Porcupine Seabight (north‐east Atlantic Ocean; continental slope) and a transect along the Kenyan coast (Indian Ocean; shallow lagoon). Methods In the north‐east Atlantic, dead coral fragments, sponge skeletons and sediment were collected with a boxcorer. Along the Kenyan coast, dead coral fragments and coral gravel were collected during snorkelling and skin diving. Only nematodes belonging to the families Epsilonematidae and Draconematidae were considered. Community structure was analysed using multivariate techniques. Biodiversity was represented via rarefaction curves. Additive partitioning of species diversity was conducted. Turnover between microhabitats within locations and between locations within microhabitats were compared in a ternary plot. Results Twelve epsilonematid and five draconematid species were found in the Porcupine Seabight. In Kenya, 39 epsilonematid and 20 draconematid species were distinguished. Three species were found at both sampling locations. A table with the known distribution of all currently described species encountered in our study area is provided. At both sampling locations, the communities on coral fragments were significantly different from those in the other microhabitats, and were most diverse. In Kenya, species richness was mainly determined by local diversity and by turnover between localities. The contribution of β‐diversity decreased when abundance data were analysed. Turnover between microhabitats and between coral samples from different localities was higher than turnover between locations for gravel samples. Main conclusions Coral fragments were recognized as favourable substrata for typically epifaunal nematodes. Species‐specific habitat preferences were explained by finely tuned morphological adaptations. Our results suggest that cosmopolitan species could well be cryptic species, and this explanation for the existence of morphologically identical nematodes in geographically distant areas is weighed up against other plausible explanations. Coral degradation zones are an important source for new species of Epsilonematidae and Draconematidae. The addition of sampling locations contributed to the total number of species, although the added species were generally rare.     

Tag location and risk assessment for passive integrated transponder‐tagging passerines

Understanding changes in body temperature is central to several fields in biology, but determining these changes accurately without harming or restraining individuals can be challenging, particularly for small species. We tested first whether body temperature readings differed between passive integrated transponder (PIT) tags injected subcutaneously inter‐scapulae (i.e. solely through the skin) and intra‐peritoneally (through the skin and abdominal muscle wall) and, secondly, whether intra‐peritoneal tag injuries differed among three weight classes of passerines. We found no significant difference in body temperature readings between subcutaneous inter‐scapulae and intra‐peritoneal PIT‐tags, and observed that the intra‐peritoneal injection of PIT‐tags may cause adverse effects among smaller (<25 g) birds. Our findings suggest a reduced gradient between core and peripheral body temperature in small species, which to the best of our knowledge has not yet been quantified. We further show that the risk of detrimental injury was greatest in small species, and thus recommend implanting PIT‐tags subcutaneously between the scapulae for smaller birds.     

Assessing population parameters and trends of Guiana dolphins (Sotalia guianensis): An eight‐year mark‐recapture study

This study represents the first attempt to study the population dynamics of Guiana dolphins (Sotalia guianensis), by evaluating a set of demographic parameters. The population of the Caravelas River estuary, eastern Brazil, was systematically monitored through a long‐term mark‐recapture experiment (2002–2009). Abundance estimates revealed a small population (57–124 dolphins), comprised of resident dolphins and individuals that temporarily leave or pass through the study area. Temporary emigration from the estuary to adjacencies (γ″= 0.33 ± 0.07 SE) and return rate (1 ?γ′= 0 .67) were moderate and constant, indicating that some dolphins use larger areas. Survival rate (?= 0.88 ± 0.07 SE) and abundance were constant throughout the study period. Power analysis showed that the current monitoring effort has high probability of detecting abrupt population declines (1 ?β= 0.9). Although the monitoring is not yet sensitive to subtle population trends, sufficient time to identify them is feasible (additional 3 yr). Despite such apparent stability, this population, as many others, inhabits waters exposed to multiple human‐related threats. Open and closed population modeling applied to photo‐identification data provide a robust baseline for estimating several demographic parameters and can be applied to other populations to allow further comparisons. Such synergistic efforts will allow a reliable definition of conservation status of this species.     

Considering sampling bias in close‐kin mark–recapture abundance estimates of Atlantic salmon

Genetic methods for the estimation of population size can be powerful alternatives to conventional methods. Close‐kin mark–recapture (CKMR) is based on the principles of conventional mark–recapture, but instead of being physically marked, individuals are marked through their close kin. The aim of this study was to evaluate the potential of CKMR for the estimation of spawner abundance in Atlantic salmon and how age, sex, spatial, and temporal sampling bias may affect CKMR estimates. Spawner abundance in a wild population was estimated from genetic samples of adults returning in 2018 and of their potential offspring collected in 2019. Adult samples were obtained in two ways. First, adults were sampled and released alive in the breeding habitat during spawning surveys. Second, genetic samples were collected from out‐migrating smolts PIT‐tagged in 2017 and registered when returning as adults in 2018. CKMR estimates based on adult samples collected during spawning surveys were somewhat higher than conventional counts. Uncertainty was small (CV < 0.15), due to the detection of a high number of parent–offspring pairs. Sampling of adults was age‐ and size‐biased and correction for those biases resulted in moderate changes in the CKMR estimate. Juvenile dispersal was limited, but spatially balanced sampling of adults rendered CKMR estimates robust to spatially biased sampling of juveniles. CKMR estimates based on returning PIT‐tagged adults were approximately twice as high as estimates based on samples collected during spawning surveys. We suggest that estimates based on PIT‐tagged fish reflect the total abundance of adults entering the river, while estimates based on samples collected during spawning surveys reflect the abundance of adults present in the breeding habitat at the time of spawning. Our study showed that CKMR can be used to estimate spawner abundance in Atlantic salmon, with a moderate sampling effort, but a carefully designed sampling regime is required.     

Larval fish collected from sound‐scattering layers in an offshore tropical area

The composition of the larval fish assemblage in the sound‐scattering layer of the continental shelf waters off the coast of south‐eastern Brazil (12 and 22° S), a research project that is part of the Brazilian programme Avaliação do Potencial Sustentável de Recursos Vivos na Zona Econômica Exclusiva (REVIZEE), is described. Samples were collected during daylight hours and at dusk at five oceanographic stations in the winter of 1999 using an Isaacs‐Kidd Midwater Trawl (IKMT). The oceanographic stations were chosen based on the detection of plankton layers by acoustic observation. A total of 2192 larval fish were identified, comprising 52 families and 62 species. Maurolicus stehmanni (Sternoptychidae) was the most abundant species found within the study area, comprising 18·5% of all identified larvae, followed by Psilotris celsus (Gobiidae) at 10·9%.     

Effects of flipper bands and injected transponders on the survival of adult Little Penguins Eudyptula minor

Tagging is essential for many types of ecological and behavioural studies, and it is generally assumed that it does not affect the fitness of the individuals being examined. However, the tagging of birds has been shown to have negative effects on some aspects of their lives. Here we investigate the influence of tagging on apparent survival. We examined the effects of flipper bands and injected transponders on the apparent survival of adult Little Penguins by comparing the survival probabilities of 2483 Little Penguins marked at Phillip Island, Australia, between 1995 and 2001 in one of three ways: with bands, with transponders or with both. The design of the study and our method of analysis allowed us to estimate tag loss and ensured that tag loss did not bias the survival estimates. Birds marked with flipper bands had lower survival probabilities than those marked with transponders (with apparent survival probabilities in the first year after tagging of 75% for banded birds and 80% for birds fitted with transponders, and in subsequent years of 87% for banded birds and 91% for birds fitted with transponders). We estimated both band and transponder loss probabilities for the first time, and found that transponder loss probabilities were substantially higher than band loss probabilities, particularly in the first year after marking when the tag loss probability was 5% for transponders and 0.7% for bands. Survival probabilities were lower in the first year after marking than in subsequent years for all birds. Studies of penguins that have used flipper bands to identify individuals may have underestimated annual adult survival probabilities, as banded penguins were likely to have lower than average survival probabilities than those of unbanded birds. The higher annual survival probabilities of individuals marked with transponders indicate that this should be the preferred marking technique for Little Penguins. However, future studies will, like ours, need to consider the higher rates of transponder loss when estimating survival, possibly by double‐tagging some birds.     

Robustness of close‐kin mark–recapture estimators to dispersal limitation and spatially varying sampling probabilities

1. Close‐kin mark–recapture (CKMR) is a method for estimating abundance and vital rates from kinship relationships observed in genetic samples. CKMR inference only requires animals to be sampled once (e.g., lethally), potentially widening the scope of population‐level inference relative to traditional monitoring programs.
2. One assumption of CKMR is that, conditional on individual covariates like age, all animals have an equal probability of being sampled. However, if genetic data are collected opportunistically (e.g., via hunters or fishers), there is potential for spatial variation in sampling probability that can bias CKMR estimators, particularly when genetically related individuals stay in close proximity.
3. We used individual‐based simulation to investigate consequences of dispersal limitation and spatially biased sampling on performance of naive (nonspatial) CKMR estimators of abundance, fecundity, and adult survival. Population dynamics approximated that of a long‐lived mammal species subject to lethal sampling.
4. Naive CKMR abundance estimators were relatively unbiased when dispersal was unconstrained (i.e., complete mixing) or when sampling was random or subject to moderate levels of spatial variation. When dispersal was limited, extreme variation in spatial sampling probabilities negatively biased abundance estimates. Reproductive schedules and survival were well estimated, except for survival when adults could emigrate out of the sampled area. Incomplete mixing was readily detected using Kolmogorov–Smirnov tests.
5. Although CKMR appears promising for estimating abundance and vital rates with opportunistically collected genetic data, care is needed when dispersal limitation is coupled with spatially biased sampling. Fortunately, incomplete mixing is easily detected with adequate sample sizes. In principle, it is possible to devise and fit spatially explicit CKMR models to avoid bias under dispersal limitation, but development of such models necessitates additional complexity (and possibly additional data). We suggest using simulation studies to examine potential bias and precision of proposed modeling approaches prior to implementing a CKMR program.

     

Re‐examining extreme longevity of the cave crayfish Orconectes australis using new mark–recapture data: a lesson on the limitations of iterative size‐at‐age models

1. Centenarian species, defined as those taxa with life spans that frequently exceed 100 years, have long been of interest to ecologists because they represent an extreme end point in a continuum of life history strategies. One frequently reported example of a freshwater centenarian is the obligate cave crayfish Orconectes australis, with a maximum longevity reported to exceed 176 years. As a consequence of its reported longevity, O. australis has been used as a textbook example of life history adaptation to the organic‐carbon limitation that characterises many cave‐stream food webs. 2. Despite being widely reported, uncertainties surround the original estimates of longevity for O. australis, which were based on a single study dating from the mid‐1970s. In the present study, we re‐evaluated the growth rate, time‐to‐maturity, female age‐at‐first‐reproduction and longevity of O. australis using a mark–recapture study of more than 5 years based upon more than 3800 free‐ranging individuals from three isolated cave streams in the south‐eastern United States. 3. The results of our study indicate that accurate estimates of the longevity of O. australis are ≤22 years, with only a small proportion of individuals (<5%) exceeding this age. Our estimates for female time‐to‐maturity (4–5 years) and age‐at‐first‐reproduction (5–6 years) are also substantially lower than earlier estimates. 4. These new data indicate that the age thresholds for life history events of O. australis are comparable to other estimates for a modest assemblage of cave and surface species of crayfish for which credible age estimate exists, suggesting that a cave environment per se is not required for the evolution of extreme longevity in crayfish.     

Dispersal of single‐ and double‐brood populations of the European earwig,Forficula auricularia: a mark‐recapture experiment

Quantitative information on dispersal of insects should be taken into consideration for making efficient pest management decisions. Such information was not available for the European earwig, Forficula auricularia L. (Dermaptera: Forficulidae), an important biocontrol agent in fruit orchards. A mark‐recapture experiment was carried out in Belgian orchards, where marked earwigs were released at a single point and recaptured after 1 month. Dispersal from this release point was analysed using an analytical formula of a simple diffusion model with disappearance (e.g., as a result of death) derived by Turchin & Thoeny (1993; Quantifying dispersal of southern pine beetles with mark‐recapture experiments and a diffusion model. Ecological Applications 3: 187) . The cumulative number of recaptured earwigs as a function of the distance of release was used to fit the model and estimate parameters. A derived expression, in terms of these parameters, was used to estimate the frequency distribution of the population, as the radius of a circle enclosing various proportions of the earwigs’ dispersal distances. In Belgium, populations of the European earwig can have two life‐history strategies, single‐ (SBP) and double‐brood populations (DBP). Therefore, mark‐recapture experiments were carried out on both population types. We fitted data from SBP (n = 10) and DBP (n = 16) successfully in both the diffusion model and in an exponential curve. Because of the biological relevance, estimates of the diffusion model were used for calculating the frequency distributions. Males and females dispersed the same distances. No differences were found between orchards with different spatial structures (apple and pear). According to literature data, mobility of earwigs is very low compared with other arthropods, which has consequences for the efficiency of biocontrol interventions, like mass releases of earwigs or the use of hedgerows for the establishment of healthy (source) populations. Quantitative results revealed that earwigs of SBP dispersed four times further than earwigs of double‐brood populations. For instance, 95% of the population remained within a radius of 28.6 m in SBP and 7.54 m in DBP.     

Use of PIT tags to assess individual heterogeneity of laboratory‐reared juveniles of the endangered Cumberlandian combshell (Epioblasma brevidens) in a mark–recapture study

The federally endangered Cumberlandian combshell (Epioblasma brevidens) was propagated and reared to taggable size (5–10 mm), and released to the Powell River, Tennessee, to augment a relict population. Methodology using passive integrated transponder (PIT) tags on these mussels greatly facilitated the detection process. The overall mean detection probability and survival rate of released individuals reached 97.8 to 98.4% and 99.7 to 99.9% (per month), respectively, during nine successive recapture occasions in the 2‐year study period, regardless of seasonality. Nonhierarchical models and hierarchical models incorporating individual and seasonal variations through a Bayesian approach were compared and resulted in similar performance of prediction for detection probability and survival rate of mussels. This is the first study to apply the mark–recapture method to laboratory‐reared mussels using PIT tags and stochastic models. Quantitative analyses for individual heterogeneity allowed examination of demographic variance and effects of heterogeneity on population dynamics, although the individual and seasonal variations were small in this study. Our results provide useful information in implementing conservation strategies of this faunal group and a framework for other species or similar studies.     

Estimability of migration survival rates from integrated breeding and winter capture–recapture data

Long‐distance migration is a common phenomenon across the animal kingdom but the scale of annual migratory movements has made it difficult for researchers to estimate survival rates during these periods of the annual cycle. Estimating migration survival is particularly challenging for small‐bodied species that cannot carry satellite tags, a group that includes the vast majority of migratory species. When capture–recapture data are available for linked breeding and non‐breeding populations, estimation of overall migration survival is possible but current methods do not allow separate estimation of spring and autumn survival rates. Recent development of a Bayesian integrated survival model has provided a method to separately estimate the latent spring and autumn survival rates using capture–recapture data, though the accuracy and precision of these estimates has not been formally tested. Here, I used simulated data to explore the estimability of migration survival rates using this model. Under a variety of biologically realistic scenarios, I demonstrate that spring and autumn migration survival can be estimated from the integrated survival model, though estimates are biased toward the overall migration survival probability. The direction and magnitude of this bias are influenced by the relative difference in spring and autumn survival rates as well as the degree of annual variation in these rates. The inclusion of covariates can improve the model's performance, especially when annual variation in migration survival rates is low. Migration survival rates can be estimated from relatively short time series (4–5 years), but bias and precision of estimates are improved when longer time series (10–12 years) are available. The ability to estimate seasonal survival rates of small, migratory organisms opens the door to advancing our understanding of the ecology and conservation of these species. Application of this method will enable researchers to better understand when mortality occurs across the annual cycle and how the migratory periods contribute to population dynamics. Integrating summer and winter capture data requires knowledge of the migratory connectivity of sampled populations and therefore efforts to simultaneously collect both survival and tracking data should be a high priority, especially for species of conservation concern.