Biological Intercept Research Articles

Age and Growth of the Horse Clam Tresus keenae in Seto Inland Sea and Ise Bay, Western Japan

The age and growth of horse clams Tresus keenae from Seto Inland Sea (SIS) and Ise Bay, western Japan, were investigated using a water-based marking pen on the edge of sectioned shells, after which unstained translucent zones at the chondrophore could be clearly observed. The translucent zone was formed once per year during autumn. The ages of all the samples were determined. The most frequent shell length (SL) in SIS and Ise Bay populations were 100–120 mm and 120–140 mm, respectively and mainly consisted of 3-y-old and 4-y-old clams, respectively. Clams in the SIS were found to be younger by about 1 y and 20 mm smaller on average than the Ise Bay population. The age–SL relationships of clams from each area were analyzed, using the original von Bertalanffy growth function (VBGF), a VBGF with a biological intercept, and the Gompertz growth function. The original VBGF showed the best fit with the SIS dataset, whereas the Gompertz growth model showed the best fit with Ise Bay clams. The parameters for each growth model were significantly different between SIS and Ise Bay, which may be due to clams younger than 2 y and smaller than 80 mm SL that were present only in the samples from SIS. Faster growth rate of the VBGF in Ise Bay than that in SIS would be affected by higher water temperature during the season of rapid growth.

Decoupling of otolith and somatic growth during anadromous migration in a northern salmonid

We assessed the fish length – otolith length relationship (FL–OL) in Dolly Varden (Salvelinus malma malma) to verify proportional growth. A decoupling was detected during first ocean migration where fish growth was occurring at a greater rate than otolith growth. Because of this decoupling, the application of traditional back-calculation models overestimated the size-at-age in premigratory char. We developed modified back-calculation equations from existing traditional models to account for this decoupling based on discontinuous piecewise regressions. The new biological intercept breakpoint method (BI–BP) provided the most accurate representation of fish size-at-age throughout all life history stages when compared with known size-at-capture values in fish. The decoupling indicates that factors other than somatic growth are important for otolith accretion. Physiological changes during smoltification likely alter calcium uptake and thereby affect calcium deposition rates on otoliths during this short but biologically critical time period of life history. It is probable that species exhibiting similar complex ontogenetic shifts in life history will likely exhibit decoupling to some extent in the FL–OL relationship.

A new proportionality-based back-calculation approach, which employs traditional forms of growth equations, improves estimates of length at age

The performance of a new proportionality-based back-calculation approach, describing the relationship among length, otolith size, and age using traditional growth curves and assuming a bivariate distribution of deviations from those curves, was evaluated. Cross-validation was used for six teleost species to compare predictions of expected lengths or otolith sizes at age, given otolith size or length, respectively, with those of other proportionality-based approaches that incorporate age. For four species, and particularly Acanthopagrus butcheri when using a biological intercept, better estimates were produced using the new model than were produced using the regression equations in the other back-calculation approaches. Back-calculated lengths for A. butcheri estimated using this model were more consistent with observed lengths, particularly when employing a biological intercept, than those obtained using other proportionality-based approaches and also a constraint-based approach known to produce reliable estimates. By selecting somatic and otolith growth curves from a suite of alternatives to better describe the relationships among length, otolith size, and age, the new approach is likely to produce more reliable estimates of back-calculated length for other species.

Correlations between body length and otolith size in smallmouth bass Micropterus dolomieu Lacépède, 1802 with implications for retrospective growth analyses

Reconstructing individual growth history from analysis of increments in otoliths, scales, or spines can provide information on past growth responses to environmental variation, which in turn can be useful for predicting population-level response to climate change. The objective of this study was to examine correlations between body length and different metrics of otolith size for Micropterus dolomieu. Three metrics corresponding to commonly-used microstructural and ultrastructural otolith dimensions were measured using image analysis of digital micrographs from a sample of 214 M. dolomieu ranging from 115 to 438 mm total length collected in 2011–2013. It was found that anteroposterior length of whole otoliths provided much improved regression relationships with body size as well as ease of data collection and faster sampling throughput compared with microstructural measures from polished sections. When applying these metrics to reconstruct growth history the biological intercept model generally produced more reasonable back-calculated estimates of length-at-age, although this was not consistent across all otolith metrics. Results suggest that whole otolith measures should be employed due to efficiency of data collection and greater reliability for reconstructing growth history in M. dolomieu.

Can backcalculation models unravel complex larval growth histories in a tropical freshwater fish?

This experimental study compared the precision and accuracy of the biological intercept (BI), modified fry (MF) and time-varying growth (TVG) backcalculation models in estimating the early growth of the tropical freshwater purple-spotted gudgeon Mogurnda adspersa. Larvae were reared up to 41 days post hatching under two temperatures and four different feeding regimes. Food and temperature treatments induced complex growth profiles among fish, and although total length (LT ) and otolith radius were related under all conditions, some uncoupling was evident in the otolith-somatic-growth (OSG) relationship of fish subjected to periods of changing food availability. Furthermore, otolith growth was found to be significantly influenced by temperature, but not by food availability. Analysis of backcalculation residuals by linear mixed effects modelling revealed that BI and TVG were equally precise in predicting somatic growth, with the highest accuracy provided by TVG. The performance of all the three models declined as the OSG relationship weakened under low-food conditions, with maximum errors estimated to be 39, 60 and 36% of observed LT for the BI, MF and TVG models, respectively. The need for careful validation of backcalculation models is emphasized when examining fishes subjected to variable environmental conditions, and when exploring the differential influence of temperature and food on fish LT and otolith growth.

Validating Back‐Calculation Models Using Population Data

AbstractOtolith back‐calculation, an estimation of size and growth at some previous age, is a valuable and widely used method of tracking the traits of surviving individuals. Although numerous back‐calculation models have been developed, the accuracy of model prediction is rarely assessed before using a model on wild populations. Using the Atlantic Silverside Menidia menidia, we tested the precision of four commonly used back‐calculation models (body proportional hypothesis, modified Fry, biological intercept, and time‐varying growth). We calculated the moments of the observed length frequency distribution (mean, variance, skewness, and kurtosis) and compared them with the moments of the back‐calculated length frequency distribution predicted by each model. We also compared how the most accurate back‐calculation model changed under various scenarios of size‐selective mortality and found that bias in back‐calculation could not be explained by size‐selective mortality. The differences between functional forms over a wide range of fish sizes were slight for the biological intercept and modified Fry models, whereas the time‐varying growth and body proportional hypothesis models differed considerably. We found that all models performed well for at least one measure of accuracy. However, the modified Fry model was the most accurate overall when back‐calculating to the observed population moments.

Otolith micro structure analysis of rainbow trout alevins (Oncorhynchus mykiss) under rearing conditions

Otolith microstructure (MO) analysis was used to back-calculate growth patterns from hatching to the yolk-sac absorption in Rainbow trout alevins ( Oncorhynchus mykiss ), under experimental conditions, from winter to spring in Central-Chile. MO showed the following main features: (i) occurrences of multiple primordia in the central region of otolith (MP); (ii) several increments (22 ± 3 rings) before a prominent hatch check surrounding MP and (iii) existence of a very distinctive check associated to yolk-sac absorption. Further findings were the validation of daily periodicity of micro-increments and a significant linear relationship ( P < 0.001; r² = 0.91) between the maximum otolith length (MOL) and total length (TL) of alevins. The linear MOL-TL relationship validated the use of the biological intercept method to back-calculate daily growth rates. Growth rates profiles followed a decreasing trend from hatching to the end of yolk-sac period (16 ± 1 days), ranging from 0.34 mm d -1 to 0.22 mm d -1 (0.30 ± 0.037). MO analysis demonstrated to be a powerful tool in back-calculating growth patterns of alevins once they had absorbed their yolk-sac.

A novel length back-calculation approach accounting for ontogenetic changes in the fish length – otolith size relationship during the early life of sprat (Sprattus sprattus)

An individual-based length back-calculation method was developed for juvenile Baltic sprat ( Sprattus sprattus ), accounting for ontogenetic changes in the relationship between fish length and otolith length. In sprat, metamorphosis from larvae to juveniles is characterized by the coincidence of low length growth, strong growth in body height, and maximal otolith growth. Consequently, the method identifies a point of metamorphosis for an individual as the otolith radius at maximum increment widths. By incorporating this information in our back-calculation method, estimated length growth for the early larval stage was more than 60% higher compared with the result of the biological intercept model. After minimal length growth during metamorphosis, we found the highest increase in length during the early juvenile stage. We thus located the strongest growth potential in the early juvenile stage, which is supposed to be critical in determining recruitment strength in Baltic sprat.

Variability in fish size/otolith radius relationships among populations of Chinook salmon

Back-calculation of growth trajectories from otolith microstructure is a valuable tool for understanding mechanisms underlying variability in growth among fish populations. We analyzed fish length/otolith radius relationships for Snake River spring/summer Chinook and Snake River fall Chinook salmon, listed as separate “Evolutionarily Significant Units” (ESUs) under the US Endangered Species Act, to determine whether these ESUs shared relationships. In addition, we analyzed otoliths from seven separate populations within the Snake River spring/summer Chinook ESU to assess the variability in relationships among populations, which are much more closely related than ESUs. We also examined several potential functional forms for the equations. We found that the separate ESUs had significantly different fish length/otolith radius relationships, but that variability in otolith growth rate could not explain the difference. Relationships among populations within the spring/summer Chinook ESU did not vary nearly as much as those between ESUs. The quadratic model and the power model fit the data equally well, and constraining these models to pass through a biological intercept (estimated fish length and otolith radius at hatching) resulted in only a slight decrease in model fit. To test the ability of the models to back-calculate fish lengths, we predicted the length at tagging for 17 PIT-tagged fall Chinook that were measured at release and at recapture. The back-calculation demonstrated little bias (<1 mm FL, on average) and relatively small standard deviation (∼3.5 mm) for the best model. When we repeated the back-calculation with data from both ESUs combined, bias increased substantially (to 15 mm FL), demonstrating the importance of determining the proper taxonomic level at which to combine data within a species.

Accuracy and Precision of Estimates of Back‐Calculated Channel Catfish Lengths and Growth Increments Using Pectoral Spines and Otoliths

AbstractBack‐calculation of lengths at previous ages using measurements of growth increments on the bony structures of fish is a common practice, yet studies validating this procedure are few. Our objective was to determine the accuracy and precision of back‐calculated lengths and the last growth increment for channel catfish Ictalurus punctatus using pectoral spines and otoliths. In recent studies, the last growth increment has been related to the length of the fish at the start of the growing season to determine size‐specific growth. Growth increments on basal sections of pectoral spines were measured along three radii—posterior (SP), anterior (SA), and lateral (SL)—and otoliths were measured along the ventral radius by three independent readers. Back‐calculated lengths derived from eight models (biological intercept, body‐proportional hypothesis [BPH] linear, BPH nonlinear, Dahl–Lee, Fraser–Lee, Morita–Matsuishi, scale‐proportional hypothesis [SPH] linear, and SPH nonlinear) for each bony structure radius were compared with the actual growth histories of captive channel catfish to determine the best model and radius (for pectoral spines) for the two bony structures. The SPH linear model for SL provided the most accurate data for pectoral spines and was also appropriate for otoliths. Back‐calculated lengths and last growth increments were considerably more accurate and precise for SL than for otoliths. The SPH linear model provided an initial length–last growth increment relationship that was similar to the observed relationship for SL but not for otoliths. We also estimated last growth increments and the initial length–last growth increment relationship from the traditionally used Dahl–Lee model for SP and found that these estimates were similar to those derived from the SPH linear model for SL. We recommend using the SPH linear model for SL to estimate length‐at‐age and growth increment data. However, the Dahl–Lee model for SP also provides reasonable estimates of the last growth increment.

Back-calculation of previous fish size using individually tagged and marked Atlantic cod (Gadus morhua)

The performance of five back-calculation (B-C) models was tested with individually tagged and multiple alizarin-marked Atlantic cod ( Gadus morhua ) reared at seasonally varying water temperature and food regimes over a 10-month period. The otoliths were transversely sectioned and the otolith growth between marks was measured along the dorsal, distal, and ventral radii and across the otolith width. Observed fish lengths at each marking time were compared with back-calculated lengths using linear and nonlinear scale and body proportional hypotheses (SPH and BPH) and biological intercept (BI) models. Measurements along the dorsal and distal radius with SPH and BI provided more accurate fish length estimates but with lower precision, whereas measurements of the ventral radius consistently produced greater overestimations by any model. Otolith width measurements produced moderately overestimated fish length estimates but with the highest precision and were significantly affected by temperature in all models. Certain combinations of model and otolith dimension were more sensitive to the length of the back-calculation time interval, whereas varying feeding regime induced temporary biases only. The selection of B-C model and otolith dimension thus depends not only on the environmental conditions that the fish experience, but also on the requirements of the application for which the B-C is used.

The back-calculation of size and growth from otoliths: Validation and comparison of models at an individual level

Multiple internal and external tagging experiments tested the applicability of five back-calculation models (Biological Intercept, Modified-Fry, Body Proportional Hypothesis, Time-Varying Growth, and an Age-Effects model) as predictors of individual growth trajectories of two marine cleaning gobies, Elacatinus evelynae and E. prochilos, that were raised in aquaria under conditions that resulted in variable growth. Mixed-effect model analyses of longitudinal records of otoliths and somatic growth collected at the individual level revealed that E. evelynae and E. prochilos produced daily increments on their otoliths for up to two months post-settlement and that the Modified-Fry model provided the most accurate size-at-age estimates despite the presence of age, growth and time-varying growth effects in the dataset. Very large errors in predicted size were produced by the Age-Effects model. The four other back-calculation models all provided slightly biased estimates of back-calculated size-at-age, with the Modified-Fry model providing the least biased estimates. Regardless of bias, both experimental and theoretical evidence indicated that back-calculated size was a better proxy of fish length than otoliths radius. Relationships between fish length and otoliths radius were allometric at the level of individuals, which explained why the Modified-Fry model performed better. However, this allometry was undetectable at the population level. This study represents the first attempt to validate modern back-calculation models using longitudinal data collected and analysed at the individual level. Our results suggest the use of the Modified-Fry model as a conservative approach in routine back-calculations of fish size at age from otoliths.

Effects of river flow on larval growth and survival of Japanese seaperch Lateolabrax japonicus (Pisces) in the Chikugo River estuary, upper Ariake Bay

The abundance and growth history of larval and juvenile Japanese seaperch Lateolabrax japonicus were investigated in the Chikugo River estuary, upper Ariake Bay, from 1990 to 2000. Growth during the larval period (up to 15 mm standard length, LS, the size at recruitment into the estuary) was backcalculated using sagittal otolith microstructures by the biological intercept method. Growth rates in length declined at body sizes &gt;14 mm LS. High freshwater discharge through the Chikugo River was associated with high temperatures of the upper Ariake Bay where the larvae spend their planktonic life. Mean larval stage duration (days) from hatch to 15 mm (D15) varied between 48·8 and 76·2 days and was inversely correlated with the estimated mean temperature history [mean daily temperature (° C) experienced by the larvae during the period from hatch to 15 mm, T15]. Mean abundance (number m−2) of larvae and juveniles was highest in years when T15, D15 and freshwater discharge were at intermediate levels. Although the abundance was not correlated with either of these variables, an exponential relationship between abundance and D15 was found when data collected during the highest river discharge years (1990, 1991 and 1998) were excluded. The increase in freshwater discharge through the Chikugo River probably had the potential to enhance or diminish Japanese seaperch recruitment in two ways: 1) it could increase recruitment probability by increasing temperature and larval growth and 2) high river flow also had the potential to decrease the probability of immigration into the river by increasing larval seaward dispersion, predation due to decreased turbidity and starvation due to decreased zooplankton prey abundance in the estuary.

Growth-dependent recruitment of Pacific bluefin tuna Thunnus orientalis in the northwestern Pacific Ocean

To estimate the survival process of Pacific bluefin tuna Thunnus orientalis during the larval period, estimated growth histories were compared between larvae collected in late spring and juveniles collected in the boreal summer of 2004, which were considered to be survivors of the larval cohorts. Larval tuna (3.3 to 9.6 mm standard length, SL) were collected from mid-May to early June around the Ryukyu Islands, northwestern Pacific Ocean, and juvenile tuna were collected offshore of Kochi and Nagasaki prefectures in July-August. Preflexion, flexion and postflexion larvae were col- lected, and their ages ranged from 4 to 18 d. Back-calculated SLs by the biological intercept method showed that larval tuna in the postflexion phase were larger-at-age than preflexion and flexion larvae, suggesting that only larger and faster growing larvae were able to survive to the postflexion phase. The logarithms of otolith radii (ln OR: proportional to SL) of larvae with slower growth and development were smaller than the minimum ln OR of surviving juvenile tuna, which indicated the smallest possible size required for larvae to successfully recruit to the fishery. These results indicate that the survival of larvae of Pacific bluefin tuna depends largely on size and growth rates during early life history.

Patterns of growth in the early life history of the round herring Etrumeus teres

Early life history traits of young‐of‐the‐year (YOY) round herring Etrumeus teres, caught in Tosa Bay (south‐western Japan), were studied using otolith microstructure analysis for the 2000–2003 year classes. Hatch dates ranged from October to March, and were restricted to either autumn or winter within each year class. YOY ranged from 50 to 123 mm total length (LT) and from 57 to 192 days in age. The relationship of LT to otolith radius was linear. Individual growth rates (GI) were backcalculated between the 70th and 150th days (the size range of most YOY caught) using the biological intercept method. GI ranged from 0·3 to 1·4 mm day−1 and decreased in most cases as season progressed irrespective of year class, although GI in winter cohorts were significantly higher than in autumn cohorts. Otolith growth rates (GO) ranged from 2·13 to 12·25 μm day−1 for autumn spawned YOY and from 3·12 to 12·41 μm day−1 for YOY spawned in winter. The GO trajectories followed three consistent patterns: (1) an increase in increment widths after first feeding through the second week of larval life, then (2) a plateau in increment spacing before increment widths increased again until reaching the maximum growth rate, followed by (3) a gradual decrease in increment widths until the end of the fifth month. The three stages occurred irrespective of spawning season, although YOY spawned in October and December had higher GO during stages (1) and (2) than YOY spawned in February and March, whereas higher GO was observed for late‐winter cohorts in stage (3). Otolith growth from YOY spawned in December and January showed an intermediate pattern between YOY hatched in the early autumn (October to December) and late winter (February to March). The GO trajectories were cross‐matched to the calendar date to estimate time series of otolith growth rates (GOTS) for each year. A parabolic trend was found with maximum GOTS in autumn and spring and minimum values in winter. This trend was significantly correlated to daily sea surface temperature variations. The differences in otolith growth trajectories suggest that the otolith microstructure of E. teres may be used as a natural tag for identifying autumn and winter spawned cohorts.

A new model of growth back-calculation incorporating age effect based on otoliths

We developed a simple back-calculation model that includes the age effect in which otolith size increases continuously during no-growth periods. To evaluate the validity of our proposed model, we back-calculated the past fish lengths and growth rates using the new model and seven traditional back-calculation models (scale-proportional hypothesis (SPH), body-proportional hypothesis (BPH), Fraser–Lee, biological intercept, nonlinear SPH, nonlinear BPH, and modified Fry) using the otoliths of individually tag-recaptured white-spotted char (Salvelinus leucomaenis). The estimated fish lengths corresponded well to observed fish lengths for simple traditional (SPH, BPH, and Fraser–Lee) and the new models. However, the back-calculated growth rates did not correspond to observed growth rates except for the new model. All previous models had considerable bias; growth rates of slow-growing fish were overestimated. As our model incorporating the age effect did not show such bias, this bias would be attributed to the age effect. Our proposed back-calculation model incorporating the age effect should be useful to estimate past growth rates at the individual level.

Growth of larval and early juvenile Japanese anchovy, Engraulis japonicus, in the Kuroshio‐Oyashio transition region

Larvae, juveniles, and adults of Japanese anchovy, Engraulis japonicus, were distributed throughout the Kuroshio‐Oyashio transition region off northern Japan as far offshore as 170°E in 1996 and 1997. The growth trajectories of individual larvae and early juveniles were backcalculated using the biological intercept method based on the allometric relationship between otolith radius and somatic length. Mean larval growth rates ranged from 0.49 to 0.71 mm day–1 in the transition region, and were comparable to those reported from the Pacific coastal waters of central Japan, which is the principal distribution range of E. japonicus. In terms of growth, the Kuroshio‐Oyashio transition region seemed to be a favourable nursery area for larval E. japonicus. Larval growth tended to decline from the inshore to the offshore waters in the transition region. Thermal conditions did not show an inshore–offshore trend in the survey area and did not explain the longitudinal trend in growth rates.

Comparison of techniques of back-calculation of growth and settlement marks from the otoliths of three species ofDiplodusfrom the Mediterranean Sea

We developed a model of back-calculation of fish size from otoliths that could accommodate both changes in the relationship between otolith and somatic growth that occur through time and variation in growth rates among individuals. We used this model to back-calculate estimates of size and growth from otoliths of three species of Diplodus from the Mediterranean Sea. The outcomes of our model were compared with those of three other models and with growth curves estimated directly from populations of fish in the field. We found that our new model produced estimates of size-at-age that were closer to those observed in the field than the biological intercept, time-varying growth, and body proportional models. Comparison of profiles of increment width from otoliths of newly settled and juvenile Diplodus puntazzo and Diplodus vulgaris showed that these species formed a settlement mark, where increment width declined at settlement. In contrast, a settlement mark was not evident in the otoliths of Diplodus sargus. However, settlement of all species coincided with a sharp decline in somatic growth rate. Thus, growth rate may provide a means of estimating the timing of settlement in species that do not display a marked change in increment width.

Comparison of somatic growth and otolith increment growth in laboratory-reared larvae of Pacific saury, Cololabis saira , under different temperature conditions

The relationship between somatic growth and incremental growth of otoliths of Pacific saury, Cololabis saira (Brevoort), larvae under different temperature conditions was studied in the laboratory for three age groups (0 to 9, 10 to 20 and 20 to 30 d posthatch). Larvae were incubated from hatching to 9 d at 24, 20, and 16 °C. Further, larvae initially reared at an ambient temperature of 21.7 °C were transferred to experimental temperatures of 22, 18, and 14 °C on Day 10 and reared to Day 20 and similarly from Day 20 and reared to Day 30 posthatch. Growth trajectories of larvae sampled at the end of the three experiments were back-calculated using the biological intercept method and compared to the measured values 0 and 5 d after the start of each experiment. Back-calculated knob length at the different temperatures indicated no significant difference to the measured knob lengths except for the cases at 20 °C from hatching to 9-d-old larvae and at 14 °C from 20- to 30-d-old larvae. The close correlation between somatic and otolith growth shown in this study indicated the feasibility of estimating the growth history of Pacific saury larvae using otolith readings.

Size-specific changes in amount of lipid and daily growth rate of early larval sardine, Sardinops melanostictus , in the main Kuroshio Current and its offshore waters off eastern Japan

The size-specific nutritional conditions of larval sardines, Sardinops melanostictus, from the main Kuroshio Current and its offshore waters off eastern Japan were assessed by lipid analysis. A rapid lipid analysis technique (diagnostic kits for human serum lipids) was used to measure the different lipid components of individual sardine larvae as indicators of their nutritional condition. Size-specific growth trajectories of individual larvae were estimated by the biological intercept method, and the recent daily growth rate of standard length (SL) was calculated from the 3 d outer increment width on the otolith. Relationships between the amount of larval phospholipid (PL; tissue weight indicator) and SL, and the recent daily growth rate of larva (Gr) and SL, could be expressed by the equations PL = 0.459 SL1.77 and Gr = 0.0809 SL − 0.341, respectively. There was no notable difference in these values between the two survey areas. The relationship between the amount of triglyceride (TG) and SL could be expressed allometrically (TG = 0.013 SL2.63). The relationship between the index of starvation tolerance (TG/PL) and SL could be expressed by the allometric equation TG/PL = 0.0288 SL0.865, suggesting that larger sardine have a higher starvation tolerance than smaller sardine. The TG of the 8 to 9 mm SL size-class larvae in the offshore area was higher than in the main Kuroshio Current. To test whether the TG for each larval sardine in the 8 to 9 mm SL size-class could be correlated with variables (temperature, chlorophyll a and distribution density of the sardine larvae) measured at the sampling stations, correlation analyses were performed. A highly significant negative correlation between TG and distribution density of the sardine larvae was found. A density-dependence effect seemed to influence the fluctuation of the larval storage energy component for short-term needs.