Dovi Kacev’s research while affiliated with University of California, San Diego and other places

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Publications (27)


Accounting for unobserved population dynamics and aging error in close-kin mark-recapture assessments
  • Article
  • Full-text available

February 2024

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132 Reads

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5 Citations

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Dovi Kacev

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Obtaining robust estimates of population abundance is a central challenge hindering the conservation and management of many threatened and exploited species. Close-kin mark-recapture (CKMR) is a genetics-based approach that has strong potential to improve the monitoring of data-limited species by enabling estimates of abundance, survival, and other parameters for populations that are challenging to assess. However, CKMR models have received limited sensitivity testing under realistic population dynamics and sampling scenarios, impeding the application of the method in population monitoring programs and stock assessments. Here, we use individual-based simulation to examine how unmodeled population dynamics and aging uncertainty affect the accuracy and precision of CKMR parameter estimates under different sampling strategies. We then present adapted models that correct the biases that arise from model misspecification. Our results demonstrate that a simple base-case CKMR model produces robust estimates of population abundance with stable populations that breed annually; however, if a population trend or non-annual breeding dynamics are present, or if year-specific estimates of abundance are desired, a more complex CKMR model must be constructed. In addition, we show that CKMR can generate reliable abundance estimates for adults from a variety of sampling strategies, including juvenile-focused sampling where adults are never directly observed (and aging error is minimal). Finally, we apply a CKMR model that has been adapted for population growth and intermittent breeding to two decades of genetic data from juvenile lemon sharks (Negaprion brevirostris) in Bimini, Bahamas, to demonstrate how application of CKMR to samples drawn solely from juveniles can contribute to monitoring efforts for highly mobile populations. Overall, this study expands our understanding of the biological factors and sampling decisions that cause bias in CKMR models, identifies key areas for future inquiry, and provides recommendations that can aid biologists in planning and implementing an effective CKMR study, particularly for long-lived data-limited species.

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Sea surface temperature (SST) pre and post marine heat wave. To visualize the dramatic shift in ecological conditions, we plotted average daily SSTs from (a) pre (April 1, 1996–April 1, 2014) and (b) post (April 1, 2014–April 1, 2019) marine heatwave. Average SST was dramatically elevated during and after the marine heatwave. The four sites sampled are plotted in white: (1) Point Conception, (2) San Nicholas Island, (3) San Diego Inshore, and (4) San Diego Offshore.
Co‐detection of ichthyoplankton by metabarcoding and morphological methods. Detection plot of 59 species detected via microscopy (n = 48) and metabarcoding (n = 59). Metabarcoding detected all species observed in morphological counts and 11 additional species (in bold) that were not. Gray lines indicate missing data.
Bayesian joint model improves quantitative abundance estimates. Plot of observed (uncorrected) eDNA metabarcoding derived sequencing reads against observed morphological counts (a). Observed‐predicted plot for larval counts (b) and sequence reads (c) from our joint model results. The one‐to‐one line is plotted in red and Pearson correlation coefficients (r) are reported.
Novel marine heatwave assemblages. Shifts in species modeled abundances with the onset of the marine heatwave (1996–2013 vs. 2014–2019). Synchronous increases in southern mesopelagic species and Northern Anchovy (Engraulis mordax) were observed across all stations. Stations are in rows, species in columns, and the joint model estimated change in abundance between the two ecological phases is shown as the response variable. Fisheries targets including Pacific Sardine (Sardinops sagax) and North Pacific Hake (Merluccius productus), as well as many other benthic and coastal species, had concurrent negative associations. Significant differences during and after the marine heatwave are marked with + or −.
Synchronous increase in anchovy abundance during and after marine heatwave. Model posterior estimates for larval fish abundances (larvae counts per standardized volume towed) over time at each of the four sampled stations. Joint modeling of metabarcoding and morphological counts reconstructed increases in Northern Anchovy (Engraulis mordax) during the recent Pacific Marine Heatwave and low spawning of Pacific Sardine (Sardinops sagax) over the past decade (points are means and error bars are 95% credible intervals; the shaded region is during and after the marine heatwave). Northern Anchovy abundances are in blue while Pacific Sardine abundances are in red. Sea surface temperature is plotted above the Northern Anchovy and Pacific Sardine abundances for reference.
Message in a bottle: Archived DNA reveals marine heatwave-associated shifts in fish assemblages

March 2023

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212 Reads

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8 Citations

Marine heatwaves can drive large-scale shifts in marine ecosystems, but studying their impacts on whole species assemblages is difficult. Analysis combining microscopic observations with environmental DNA (eDNA) metabarcoding of the ethanol preservative of an ichthyoplankton biorepository spanning a 23 years time series captures major and sometimes unexpected changes to fish assemblages in the California Current Large Marine Ecosystem during and after the 2014-2016 Pacific Marine Heatwave. Joint modeling efforts reveal patterns of tropicalization with increases in southern, mesopelagic species and associated declines in commercially important temperate fish species (e.g., North Pacific Hake [Merluccius productus] and Pacific Sardine [Sardinops sagax]). Data show shifts in fisheries assemblages (e.g., Northern Anchovy, Engraulis mordax) even after the return to average water temperatures, corroborating ecosystem impacts found through multiple traditional surveys of this study area. Our innovative approach of metabarcoding preservative eDNA coupled with quantitative modeling leverages the taxonomic breadth and resolution of DNA sequences combined with microscopy-derived ichthyoplankton identification to yield higher-resolution, species-specific quantitative abundance estimates. This work opens the door to economically reconstruct the historical dynamics of assemblages from modern and archived samples worldwide. K E Y W O R D S amplicon sequencing, CalCOFI, California Current Ecosystem, eDNA, ichthyoplankton, joint model, marine heatwave, quantitative metabarcoding


Two's company: first record of two free-swimming megamouth sharks, Megachasma pelagios (Lamniformes: Megachasmidae), off the California coast

March 2023

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197 Reads

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1 Citation

Environmental Biology of Fishes

On September 11, 2022, two megamouth sharks ( Megachasma pelagios ), estimated at 3.7–4.6 m TL, were observed swimming together near the surface about 39 km off the coast of San Diego, CA, USA. Megamouth sharks are rarely observed pelagic sharks, and the film from this encounter provided new insight into the social behavior of this species. We attempt to put the behavior of these two individuals into the context of past sightings, known megamouth shark biology, and with analogous behavior observed in other shark and pelagic fish species.


Accounting for population growth, intermittent breeding, and aging error in close-kin mark-recapture assessments

February 2023

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98 Reads

Obtaining robust estimates of population abundance is a central challenge hindering the conservation and management of many threatened and exploited species. Close-kin mark-recapture (CKMR) is a genetics-based approach that has strong potential to improve monitoring of data-limited species by enabling estimates of abundance, survival, and other parameters for populations that have been challenging to assess. However, CKMR models have received limited sensitivity testing under realistic population dynamics and sampling scenarios, impeding application of the method in population monitoring programs and stock assessments. Here, we use individual-based simulation to examine how unmodeled population dynamics and sampling strategy affect the accuracy and precision of CKMR parameter estimates, and present adapted models that correct the biases that arise from model misspecification. Our results demonstrate that a relatively simple CKMR model produces robust estimates of population abundance when key assumptions including annual breeding and stable population size are met; however, if strong population declines or non-annual breeding dynamics are present, a more complex CKMR model must be constructed to avoid biased parameter estimates. In addition, we show that CKMR can generate reliable abundance estimates for adults from a variety of sampling strategies, including juvenile-focused sampling where adults are never directly observed. Finally, we apply our adapted CKMR model to two decades of genetic data from juvenile lemon sharks (Negaprion brevirostris) in Bimini, Bahamas to demonstrate how juvenile-focused CKMR can be used to expand monitoring efforts for highly mobile populations. Overall, this study expands our understanding of the biological factors and sampling decisions that cause bias in CKMR models, and provides recommendations for sampling design and model construction that can aid biologists in planning and implementing an effective CKMR experiment, particularly for long-lived data-limited species.


Lateral line ablation by ototoxic compounds results in distinct rheotaxis profiles in larval zebrafish

January 2023

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107 Reads

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18 Citations

Communications Biology

The zebrafish lateral line is an established model for hair cell organ damage, yet few studies link mechanistic disruptions to changes in biologically relevant behavior. We used larval zebrafish to determine how damage via ototoxic compounds impact rheotaxis. Larvae were treated with CuSO 4 or neomycin to disrupt lateral line function then exposed to water flow stimuli. Their swimming behavior was recorded on video then DeepLabCut and SimBA software were used to track movements and classify rheotaxis behavior, respectively. Lateral line-disrupted fish performed rheotaxis, but they swam greater distances, for shorter durations, and with greater angular variance than controls. Furthermore, spectral decomposition analyses confirmed that lesioned fish exhibited ototoxic compound-specific behavioral profiles with distinct changes in the magnitude, frequency, and cross-correlation between fluctuations in linear and angular movements. Our observations demonstrate that lateral line input is needed for fish to hold their station in flow efficiently and reveals that commonly used lesion methods have unique effects on rheotaxis behavior.


Message in a Bottle: Archived DNA Reveals Marine Heatwave-Associated Shifts in Fish Assemblages

July 2022

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60 Reads

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3 Citations

Marine heatwaves can drive large-scale shifts in marine ecosystems but studying their impacts on whole species assemblages can be difficult. Here, we leverage the taxonomic breadth and resolution of DNA sequences derived from environmental DNA (eDNA) in the ethanol of a set of 23-year longitudinal ichthyoplankton samples, combining these with microscopy-derived ichthyoplankton identification to yield higher-resolution, species-specific quantitative abundance estimates of fish assemblages in the California Current Large Marine Ecosystem during and after the 2014–16 Pacific marine heatwave. This integrated dataset reveals patterns of tropicalization with increases in southern, mesopelagic species and associated declines in important temperate fisheries targets (e.g., North Pacific Hake ( Merluccius productus ) and Pacific Sardine ( Sardinops sagax )). We observed novel assemblages of southern, mesopelagic fishes and temperate species (e.g., Northern Anchovy, Engraulis mordax ) even after the return to average water temperatures. Our innovative preservative derived eDNA metabarcoding and quantitative modeling approaches open the door to reconstructing the historical dynamics of assemblages from modern and archived samples worldwide. Summary Novel quantitative abundance estimates from archived DNA reveals marine heatwave-associated shifts in fish assemblages.



Putting the Pacific marine heatwave into perspective: The response of larval fish off southern California to unprecedented warming in 2014-2016 relative to the previous 65 years California Current Ecosystem, ecosystem indicator, ecosystem modeling, ecosystem-based management, fisheries management, ichthyoplankton

February 2022

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330 Reads

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30 Citations

Global Change Biology

The 2014-2016 Northeast Pacific marine heatwave (MHW) induced the warmest 3-year period on record in the California Current Ecosystem. We tested whether lar-val fish assemblage structure, phenology, and diversity dynamics were comparable to past warming events from 1951 to 2013. First, we hypothesized, based on past observations of biological effect of warming, that mesopelagic species with southern distributions relative to southern California and Pacific sardine Sardinops sagax (a coastal pelagic species) would increase during the MHW while northern mesopelagics and northern anchovy Engraulis mordax (coastal pelagic) abundances would decline. Similar to past warming, southern mesopelagics increased and northern mesopelag-ics decreased. Unexpectedly, however, a common southern mesopelagic, Mexican lampfish Triphoturus mexicanus, was approximately three times more abundant than the previous annual high. Furthermore, whereas sardine abundance did not increase, larval anchovy abundance rose to near-record highs in summer 2016. Second, we hypothesized that fishes would spawn earlier during the MHW. Fishes did not spawn in an earlier season within a year, but five of six southern mesopelagic taxa spawned earlier than typical within winter and spring. Third, we predicted that species richness would increase moderately due to an influx of southern and exodus of northern species. Richness, however, was very high in all seasons and the highest ever during the summer as multiple species with primarily southern distributions were recorded spawning for the first time in southern California. The richness of northern species was also unexpectedly high during the MHW. Northern species likely persisted in the study area because in addition to the warm water, pockets of cold water were consistently present. If, as predicted, conditions similar to the MHW become more common as oceans warm, this unique and largely unexpected combination of fishes may reflect future biological conditions.



Lateral Line Ablation by Toxins Results in Distinct Rheotaxis Profiles in Fish

November 2021

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33 Reads

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3 Citations

Zebrafish lateral line is an established model for hair cell organ damage, yet few studies link mechanistic disruptions to changes in biologically relevant behavior. We used larval zebrafish to determine how damage via ototoxic chemicals impact rheotaxis. Larvae were treated with CuSO4 or neomycin to disrupt lateral line function then exposed to water flow stimuli. Their swimming behavior was recorded, and DeepLabCut and SimBA software were used to track movements and classify rheotaxis behavior. Lateral line-disrupted fish performed rheotaxis, but they swam greater distances, for shorter durations, and with greater angular variance than controls. Further, spectral decomposition analyses demonstrated that lesioned fish exhibited toxin-specific behavioral profiles with distinct fluctuations in the magnitude, timing, and cross-correlation between changes in linear and angular movements. Our observations support that lateral-line input is needed for fish to perform rheotaxis efficiently in flow and reveals commonly used lesion methods have unique effects on behavior.


Citations (21)


... Biases in CKMR-derived estimates of population abundance can of course arise from sources other than insufficient sampling effort (Conn et al. 2020) as suspected to be the case for the two upstream populations in our study; as described above, they can also arise from unobserved population dynamics and aging errors (Sévêque et al. 2024;Swenson et al. 2024). We have argued for the value of obtaining multiple estimates of effective and census population size and demonstrated how information on the temporal changes in effective size can be used to assess accuracy and potential error in the estimate of abundance obtained via CKMR. ...

Reference:

Temporal Variability in Effective Size (N e ) Identifies Potential Sources of Discrepancies Between Mark Recapture and Close Kin Mark Recapture Estimates of Population Abundance
Accounting for unobserved population dynamics and aging error in close-kin mark-recapture assessments

... Multiple factors can lead to differences between true biomass estimates and read count data, including those prior to amplification (e.g., mt copy number/ploidy, DNA extraction efficiency, sampling stochasticity, sample preservation) and others that influence the PCR reaction itself (e.g., PCR biases resulting from primer mismatch, inhibition, and other non-primer-mismatch sources leading to differences in amplification efficiency) [109][110][111][112][113][114][115][116]. For example, a meta-analysis by Piñol et al. (2015) [113] found that primer mismatches accounted for 75% of amplification variation in studies. ...

Message in a bottle: Archived DNA reveals marine heatwave-associated shifts in fish assemblages

... From 1976 to 2010 M. pelagios was considered rare, with only 50 individuals recorded globally during that time (Nakaya 2010). In recent years it is apparent that it is more common and widespread than previously thought, with 273 confirmed records to date across 16 countries in the Atlantic, Indian and Pacific Oceans (Yu et al. 2021;Diez et al. 2022;Skelton et al. 2023). This species is classified as Least Concern on the IUCN Red List of Threatened Species, as it is globally distributed and does not appear to be heavily impacted by fisheries (Kyne et al. 2019). ...

Two's company: first record of two free-swimming megamouth sharks, Megachasma pelagios (Lamniformes: Megachasmidae), off the California coast

Environmental Biology of Fishes

... A custom microflume (previously described in Newton et al., 2023) was used as the experimental apparatus for rheotaxis behaviour. Laminar water flow of a constant velocity was provided by a 6 V bow thruster motor (#108-01, Raboesch) inserted into the flume. ...

Lateral line ablation by ototoxic compounds results in distinct rheotaxis profiles in larval zebrafish

Communications Biology

... Apart from expanding DNA taxonomic reference databases from tissues [3], they also provide untapped genomic insights that have become more accessible with the advancement of molecular techniques [4]. Metabarcoding, in particular, allows for ecological insights, such as detecting multi-decadal community shifts from eDNA in ethanol-preserved ichthyoplankton samples [5], or tracking microevolutionary changes in the gut microbiome of 100-year-old fish specimens [6]. These are prime applications of the extended specimen concept [7], that is, a comprehensive approach to biodiversity collections that extends beyond the physical object to multiple other uses made possible by efforts such as digitization, and new attitudes towards phenotypic description such as considering holobionts [8,9]. ...

Message in a Bottle: Archived DNA Reveals Marine Heatwave-Associated Shifts in Fish Assemblages
  • Citing Preprint
  • July 2022

... Determining the impacts of ENSO climate oscillations on larval supply and larval recruitment requires appropriate longitudinal sampling on the scale of decades, a temporal sampling scale which is rare in studies of larval fishes (but see [53]). In the tropics and subtropics only a handful of longitudinal studies have examined the impact of ENSO on larval fishes, and these have been focused on relatively short temporal scales, for example, a single ENSO event [18,54,55]. ...

Putting the Pacific marine heatwave into perspective: The response of larval fish off southern California to unprecedented warming in 2014-2016 relative to the previous 65 years California Current Ecosystem, ecosystem indicator, ecosystem modeling, ecosystem-based management, fisheries management, ichthyoplankton

Global Change Biology

... Lateral line hair cell function can be measured directly by stimulation with a micro water jet (De Faveri et al., 2021). Indirect measurements are possible as well, as perturbations of the lateral line function will alter zebrafish larvae swimming behavior in a water current (Suli et al., 2012;Niihori et al., 2015;Todd et al., 2017;Tantry et al., 2022), even in an ototoxin-specific manner (Newton et al., 2022). The lateral line is also responsible for the larval startle response, an avoidance reflex upon perturbation of their surroundings (Buck et al., 2012). ...

Lateral Line Ablation by Toxins Results in Distinct Rheotaxis Profiles in Fish

... These high percentages of corals that were classified at the genus level is comparable to a study of shallow-water benthic fauna that paired eDNA sampling and sequencing using scleractinian-specific markers with collections of representative morphospecies across belt-transect surveys (West et al., 2022). When paired with systematic, regional sampling and sequencing of voucher specimens to generate reference DNA barcodes, it should be expected for marine invertebrates that a high percentage of ASVs from eDNA sequencing data will be classifiable to the genus or species levels, as observed in vertebrates (Gold et al., 2021). ...

Improving metabarcoding taxonomic assignment: A case study of fishes in a large marine ecosystem

Molecular Ecology Resources

... Creating a region-specific reference database can help prevent misidentifications to non-resident taxa (Gold et al., 2021). However, this comes with the cost of reduced sensitivity (Gold et al., 2021), for example, the inability to detect new range expansions, invasions, or species yet to be identified due to their transient use of the habitat. ...

Improving Metabarcoding Taxonomic Assignment: A Case Study of Fishes in a Large Marine Ecosystem
  • Citing Preprint
  • February 2021

... This diversity of reproductive modes has important consequences for sexual selection and sexual conflict, which in elasmobranchs can manifest as phenomena such as oophagy, coercive mating and intrauterine cannibalism [18][19][20]. Both genetic monogamy and polyandry have been reported in a number of elasmobranch taxa [21,22], stimulating debate as to the underlying evolutionary mechanisms [21,22]. Convenience polyandry (where the costs of resistance for females outweigh the costs of mating) is often assumed to underlie polyandry in this clade [22], whereas recent studies suggest that additional factors such as female choice and malemale competition are important [21]. ...

An inconvenient tooth: Evaluating female choice in multiple paternity using an evolutionarily and ecologically important vertebrate clade

Molecular Ecology