Research Article |
Corresponding author: Ken Longenecker ( klongenecker@bishopmuseum.org ) Academic editor: Sanja Matić-Skoko
© 2022 Ken Longenecker, Erik C. Franklin, Renee Hill-Lewenilovo, Watisoni Lalavanua, Ross Langston, Sangeeta Mangubhai, Susanna Piovano.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Longenecker K, Franklin EC, Hill-Lewenilovo R, Lalavanua W, Langston R, Mangubhai S, Piovano S (2022) Many immature individuals and largest size classes lacked females for three coral reef fishes (Actinopterygii) in Fiji market surveys: Implications for fishery management. Acta Ichthyologica et Piscatoria 52(1): 53-65. https://doi.org/10.3897/aiep.52.80586
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Data-limited fisheries benefit from using life-history traits as biological indicators of targeted stocks. We used histology-based reproductive analyses to estimate size at maturity, per capita egg production, and the number and biomass of immature individuals in the catch for three common coral reef fishes in Fiji market surveys during 2010–2019. We studied Lutjanus gibbus (Forsskål, 1775), Parupeneus indicus (Shaw, 1803), and Chlorurus microrhinos (Bleeker, 1854), which represent three families: Lutjanidae, Mullidae, and Scaridae, respectively. Fork length comprising 50% mature individuals for females of L. gibbus was 22.7 cm, that of P. indicus was 25.9 cm, attaining 38.0 cm for C. microrhinos. Females were rare or absent in the largest size classes of all three species. Immature fish represented up to 50% by number and 41% by biomass of the catch in market surveys, with P. indicus having the greatest immature number (8%‒50%) and biomass (6%‒41%), followed by C. microrhinos (20%‒30% by count, 11%‒18% by biomass) and L. gibbus (9%‒28% by count, 5%‒14% by biomass). Individuals ≤ 30 cm for L. gibbus and P. indicus and ≤ 45 cm for C. microrhinos were responsible for ≥ 90% of egg production per spawning. Skewed size-specific sex ratios suggested that exploitation of the largest size classes had minimal effect on overall egg production. Decreased catches of immature fishes would increase the reproductive population sizes for these species.
Chlorurus microrhinos, histology, Lutjanus gibbus, Parupeneus indicus, per capita egg production, size at maturity, weight–length relation
Coral reef fisheries supply protein to more than half of the people living in tropical coastal areas and support jobs, recreational and cultural activities. However, balancing long-term conservation of the coral reef resources with the cultural, food security, and monetary needs of coastal communities is difficult due to increasing fishing efforts, reinforced by access to new technologies and driven by expanding markets. As a result, overall decline and/or overexploitation of coral reef fish stocks has been consistently reported since the 1940s (
Fiji’s subsistence and artisanal marine fisheries generate annual landings of 27 000 t (
Two less obvious causes of mismanagement potentially leading to overexploitation are poorly defined size restrictions and the deficiency of fish reproductive biology information. A common size restriction is the minimum size limit, where fishers can only retain the fishes above a certain size—usually, the estimated length at or near maturity. This approach typically relies on the assumption that each fish has reproduced at least once in its life before being caught. This way, each fish has contributed recruitment to at least one cohort of a fished population. However, reproduction can only be achieved when both sexes are present and mature, which does not happen at the same size in sequential hermaphroditic fishes. Eleven of the fourteen families where sex exchange is known in at least one species, inhabit coral reefs (
The identification of basic reproductive biology information (e.g., size at maturity) for each population of a coral reef fishery, where catches may contain up to 200 species whose abundance change seasonally (
In this case study from Fiji, we used rapid, low-cost, on-site, histology-based reproductive analysis (
This research was approved by Fiji’s Ministry of Education, Heritage and Arts (research permit RA 19/18) and conducted in accordance with relevant guidelines and regulations. No live animals were used. The methods we used for reproductive analysis followed established, statistical methods (
Specimen acquisition and whole specimen processing. All specimens for reproductive analysis originated from Labasa in Vanua Levu and were purchased between 9 March and 25 June 2018 from fishers in fish markets (Fig.
Map of the Republic of Fiji. Specimens were obtained in Labasa from fish-market vendors and from individual fishers. Additional specimens, also originating from the northern island of Vanua Levu, were purchased from vendors at Bailey Bridge market in Suva. Shaded areas represent locations referenced in the description of market survey data.
Size-at-maturity and sexual pattern. The Dietrich’s-fixed gonad subsamples were trimmed to approximately 2 mm in each dimension, then dehydrated in alcohol (60 min in each of 50%, and two changes of 95% ethanol). Using glycol methacrylate embedding kits (HistoResin, Leica Biosystems; or JB-4, Electron Microscopy Sciences) and following manufacturer instructions, gonad subsamples were infiltrated with two changes of infiltration solution (1 h and > 8 h, respectively), transferred to embedding capsules (BEEM®, size 00), then embedded in catalyzed resin. Tissue blocks were then dehydrated for 12 h in a watertight case containing silica gel packets. Ten tissue sections (approximately 7 μm thick), distributed evenly throughout each tissue subsample, were obtained from each tissue block by serial sectioning with an MT1 Porter–Blum ultramicrotome fitted with a glass knife. Tissue sections were affixed to glass microscope slides, then stained with Toluidine Blue. Ovary sections were examined at 100× and testis sections at 400× for evidence of reproductive maturity. Guides to gamete development were used to classify ovaries (
Data analysis. We constructed WLR using log-transformed data and following established statistical protocols (
pM = (1 + e((−ln (19)(L − L50)/(L95 − L50))))−1
where pM is the predicted proportion of mature individuals at a given length (L), L50 is the length comprising 50% mature individuals, and L95 is the length comprising 95% mature individuals. We report size of transition for protogynous species as the length predicted to comprise 50% males (X50). We used logistic regression analysis of the dependent variable, proportion of males, and the independent variable, the midpoint of each 2-cm size class, to produce a sexual transition curve for protogynous species. Our regression model was:
p ♂ = (1 + e((−ln (19)(X − X50)/(X95 − X50))))−1
where p♂ is the predicted proportion of males at a given length (X), X50 is the length comprising 50% males, and X95 is the length comprising 95% males. We used chi-square (χ2) analysis to test whether overall or operational sex ratios differed from 1:1. We described size-specific sex ratios of mature-sized individuals, by plotting the percent of mature females within a size class as a function of mean length within each size class. We then used exploratory regression analysis to evaluate whether sex ratios of mature individuals varied predictably with length.
Market survey data collection. Fish market surveys were conducted between 2010‒2013 at Laqere, Bailey Bridge and Suva fish markets and within 2016‒2018 at Bailey Bridge. All markets are located in Suva on the island of Viti Levu. In general, the majority of the fishes sold at Bailey Bridge were most likely from Labasa, with a much smaller amount from Lomaiviti, those sold at Laqere were most likely from the Rewa and Tailevu areas on Viti Levu, and those sold in Suva were most likely from a diversity of locations, ranging from Labasa in the North to Kadavu in the South, with no one area being the dominant supplier (
Per capita egg production. We used size at maturity and size-specific sex ratios to estimate per capita egg production: the number of eggs produced per spawning event by an individual fish, regardless of sex. Fecundity should, in theory, be proportional to the cube of female body length (
Immature individuals in fisheries catch. We used size at maturity and weight–length relations with the length composition data for the three species from market surveys to estimate the number and biomass of immature fish in the catch. We calculated the proportion of immature fish in each 1-cm size class from the specimens collected during the 2019 market survey and used them for reproductive analysis for each market survey data set (i.e., 2010–2013, 2016–2018, 2019). The product of the proportion of immature fish by length and the weight at that length from the WLR provided an estimate of the immature biomass in the catch for each size class, which were summed to give a total immature biomass. We calculated percentages of the number and biomass of immature fish relative to the total market catch of both immature and mature fish for each species.
We estimated reproductive parameters for Lutjanus gibbus, Parupeneus indicus, and Chlorurus microrhinos using histology-based methods (Table
Summary of weight–length relations and reproductive information for four exploited reef fishes from Fiji. Lm is the length of the smallest mature individual. L50 and L95 are the lengths comprising 50% and 95% mature individuals, respectively. Lengths are in cm.
Lutjanus gibbus | Parupeneus indicus | Chlorurus microrhinos | |
---|---|---|---|
Weight–length (overall) | W = 7.55·10–6(LF)3.18 | W = 1.04·10–4(LF)2.71 | W = 1.01·10-5(LF)3.13 |
Male weight–length | — | W = 1.09·10–4(LF)2.70 | — |
Female weight–length | — | W = 3.35·10–4(LF)2.48 | — |
Male Lm | 22.5 | 21.0 | 33.7 |
Female Lm | 21.7 | 20.5 | 36.2 |
Male L50 | 23.1 | 24.2 | — |
Female L50 | 22.7 | 25.9 | 38.0 |
Male L95 | 25.3 | 30.0 | — |
Female L95 | 27.2 | 32.5 | 47.8 |
Oocyte development | Batch synchronous | Batch synchronous | Batch synchronous |
Sexual pattern | Gonochore | Gonochore | Protogynous (presumed) |
Size of transition (X50) | n/a | n/a | 40.0 |
Overall sex ratio (M:F) | 1:1.25 | 1:0.51 | 1:0.87 |
Functional sex ratio (M:F) | 1:0.95 | 1:0.27 | 1:0.49 |
Size specific sex ratios | See Fig. |
See Fig. |
See Fig. |
Lutjanus gibbus. The weight–length relation (WLR) regression parameters a and b had 95% confidence intervals of 4.90·10–6–1.16·10–5 and 3.10–3.26, respectively (r2 = 0.977, n = 155, LF range: 17.2–35.4 cm, W range: 100–960 g). Per ANCOVA results, there was no significant sex-based difference in WLRs (F = 0.60, df = 1, P = 0.441).
We examined the gonads of 49 male and 61 female L. gibbus. Photomicrographs of immature and mature gonads of both sexes are presented as supplementary information (Fig.
Histological sections of gonads of Lutjanus gibbus from Fiji. (A) Ovary of immature female (21.6 cm LF) containing only primary-growth oocytes; (B) ovary of mature female (27.3 cm LF) containing a mixture of oocyte stages including final maturation (IV); (C) testis from an immature male (22.6 cm LF) containing no tailed spermatozoa; (D) testis of a mature male (29.8 cm LF:) with tailed spermatozoa (S); scale bars = 100 μm (A and B) or 50 μm (C and D).
Spermiated testes were seen in males as small as 22.5 cm LF and all males ≥ 27.5 cm LF were mature. We estimated male L50 at 23.1 cm LF (Fig.
Reproductive information for Lutjanus gibbus from Fiji. (A) size at maturity (L50); (B) percentage of mature females, relative to all mature individuals, versus length. Females are represented by closed circles and the solid curves, males are represented by open circles and the dashed curve.
A t-test detected a sex-based bimodal size distribution in L. gibbus. The mean length of males was significantly greater than that of females (t = –6.218, df = 83, P < 0.001). However, there was no histological evidence of hermaphroditism in L. gibbus; testes did not contain a central membrane-lined lumen, and we did not detect a mixture of ovarian and spermatogenic tissue in any gonad. We classified L. gibbus as a gonochore.
Overall sex ratio in this L. gibbus population was female-biased, but not statistically different from 1:1 (Table
Parupeneus indicus. The WLR regression parameters a and b had 95% confidence intervals of 4.63·10–5–2.36·10–4 and 2.56–2.85, respectively (r2 = 0.908, n = 134, LF range: 18.9–34.1 cm, W range: 150–730 g). Per ANCOVA results, there was a significant sex-based difference in WLRs (F = 14.50, df = 1, P < 0.001). Sex-specific WLRs are presented in Table
We examined the gonads of 61 male and 32 female P. indicus. Photomicrographs of immature and mature gonads of both sexes are presented as supplementary information (Fig.
Histological sections of gonads of Parupeneus indicus from Fiji. (A) ovary of immature female (22.2 cm LF) containing only primary-growth oocytes; (B) ovary of mature female (23.6 cm LF) containing a mixture of oocyte stages including vitellogenesis (III); (C) testis from an immature male (31.5 cm LF) containing no tailed spermatozoa; (D) testis of a mature male (26.3 cm LF) with tailed spermatozoa (S); scale bars = 100 μm (A and B) or 50 μm (C and D).
A t-test detected a sex-based bimodal size distribution in P. indicus. The mean length of males was significantly greater than that of females (t = –3.536, df = 80, P < 0.001). However, there was no histological evidence of hermaphroditism in P. indicus; testes did not contain a central membrane-lined lumen, and we did not detect a mixture of ovarian and spermatogenic tissue in any gonad. We classified P. indicus as a gonochore.
Overall sex ratio in this P. indicus population was significantly male-biased (Table
Reproductive information for Parupeneus indicus from Fiji. (A) size at maturity (L50); (B) percentage of mature females, relative to all mature individuals, versus length. Females are represented by closed circles and the solid curves, males are represented by open circles and the dashed curve.
Chlorurus microrhinos. The WLR regression parameters a and b had 95% confidence intervals of 4.98·10–6–2.05·10–5 and 3.01–3.24, respectively (r2 = 0.966, n = 100, LF range: 29.6–52.2 cm, W range: 660–3300 g). Per ANCOVA results, there was no significant sex-based difference in WLRs (F = 0.00, df = 1, P = 0.982).
We examined the gonads of 47 male and 41 female C. microrhinos. Photomicrographs of immature and mature gonads of both sexes are presented as supplementary information (Fig.
Histological sections of gonads of Chlorurus microrhinos from Fiji. (A) ovary of immature female (36.3 cm LF) containing primary-growth (I) and cortical vesicle (II) oocytes, plus a conspicuous lumen (L); (B) ovary of mature female (37.1 cm LF) containing a mixture of oocyte stages including final maturation (IV); (C) testis from an immature male (38.0 cm LF) containing no tailed spermatozoa, but with a conspicuous lumen (L); (D) testis of a mature male (38.7 cm LF) with tailed spermatozoa (S); scale bars = 100 μm (A and B) or 50 μm (C and D).
Reproductive information for Chlorurus microrhinos from Fiji. (A) size at maturity (L50); (B) size of transition (X50); (C) percentage of mature females, relative to all mature individuals, versus length. Females are represented by closed circles and the solid curves, males are represented by open circles and the dashed curve.
A t-test detected a sex-based bimodal size distribution in C. microrhinos. The mean length of males was significantly greater than that of females (t = –5.471, df = 81, P < 0.001). There was some histological evidence of sex change in C. microrhinos; 17 testes contained a central membrane-lined lumen. However, we did not detect a mixture of ovarian and spermatogenic tissue in any gonad. We provisionally classify C. microrhinos as a protogynous hermaphrodite. Assuming we correctly evaluated its sexual pattern, the size of transition (X50) for C. microrhinos in Fiji was 40.0 cm LF (Fig.
Overall sex ratio in this C. microrhinos population was not statistically different from 1:1 (Table
Per capita egg production. When considering size-specific sex ratios, peak per capita egg production per spawning event was, for all species, estimated to be within a few centimeters of female L50 and less than 2/3 of the maximum length observed during market surveys (Fig.
Estimated per capita egg production per spawning event. The solid curve represents estimates when size-specific sex ratios are considered, the dashed curve represents estimates when sex ratios are assumed to be equal and invariant. (A) Lutjanus gibbus; (B) Parupeneus indicus; (C) Chlorurus microrhinos. Arrows indicate 90% cumulative egg production. Note that x- and y-axis scales vary.
Immature individuals in fisheries catch. Immature fish of the three species represented between 8%‒50% by number and 5%‒41% by biomass of the catch in market surveys (Table
The number and estimated weights of immature and mature fishes for three reef fish species from Fijian fish market surveys (years 2010–2013 and 2016–2018). The fish number and weights of the reproductive samples (year 2019) were measured.
Parameter | Lutjanus gibbus | Parupeneus indicus | Chlorurus microrhinos | ||||||
---|---|---|---|---|---|---|---|---|---|
2010 | 2016 | 2019 | 2010 | 2016 | 2019 | 2010 | 2016 | 2019 | |
Total fish No. | 443 | 169 | 163 | 215 | 12 | 141 | 180 | 65 | 101 |
Female No. | 314 | 79 | 104 | 44 | 1 | 50 | 97 | 27 | 48 |
Males No. | 129 | 90 | 59 | 171 | 11 | 91 | 83 | 38 | 53 |
Total immature No. | 123 | 16 | 44 | 60 | 1 | 71 | 54 | 13 | 22 |
Immature Female No. | 113 | 13 | 38 | 29 | 1 | 35 | 54 | 13 | 22 |
Immature Male No. | 10 | 3 | 6 | 31 | 0 | 36 | 0 | 0 | 0 |
Total W [kg] | 119.4 | 56.8 | 41.4 | 203.6 | 11.4 | 92.8 | 214.8 | 84.7 | 121.9 |
Female W [kg] | 62.8 | 19.7 | 20.0 | 25.4 | 0.6 | 27.8 | 84.0 | 24.9 | 45.5 |
Male W [kg] | 56.6 | 37.1 | 21.3 | 178.2 | 10.8 | 65.0 | 130.8 | 59.8 | 76.4 |
Total immature W [kg] | 17.1 | 2.8 | 6.0 | 33.7 | 0.6 | 38.0 | 38.4 | 9.0 | 18.0 |
Immature Female W [kg] | 15.4 | 2.3 | 5.0 | 14.8 | 0.6 | 18.0 | 38.4 | 9.0 | 18.0 |
Immature Male W [kg] | 1.7 | 0.5 | 1.0 | 18.9 | 0.0 | 20.0 | 0.0 | 0.0 | 0.0 |
We used rapid, histological methods to estimate a suite of reproductive parameters for three coral reef fishes. We acknowledge that estimates of life history parameters for high value fishery species are typically based on hundreds to thousands of specimens, often collected and compared annually or spatially. For small-scale tropical fisheries, a similar production-scale effort for life history studies is rarely feasible. The approach that we present follows a scientifically valid methodology working with relatively smaller sample sizes that provides important life history information for conservation and management guidance on coral reef species in data limited fisheries.
Our results allow comparisons of method (different methods used in the same location) and location effects (the same methods used in different regions). Table
A comparison of macroscopic (from
Lutjanus gibbus | Parupeneus indicus | Chlorurus microrhinos | |
---|---|---|---|
Macroscopic L50 | 29.8 | 32.5 | 37.5 |
Histological L50 male | 23.1 | 24.2 | — |
Histological L50 female | 22.7 | 25.9 | 38.0 |
In the absence of a robust understanding of geographic patterns of size at maturity, it would be prudent to use site-specific estimates of reproductive parameters when developing management strategies. Two of the species we analyzed in this study were the subject of histology-based reproductive analysis at other locations. Similar histology-based methods were used to study P. indicus in Papua New Guinea (
The use of rapid histology-based methods allows the identification of emergent patterns in reproduction during processing for each set of specimens. For instance, for the three species analyzed in the presently reported study, mature females are more abundant in the lower range of size classes containing mature individuals and become increasingly rare, then absent, as length increases (Figs
Size-specific sex ratios such as those we report here have two major implications for fishery conservation and management. First, with females absent from the largest size classes, fishing at or near the maximum size will have little impact on population-level egg production. Second, imposing slot limits to protect the largest individuals would direct fishing pressure toward smaller size classes which, because they comprise the highest proportions of females, are the major source of population-level egg production.
Our results suggest that protection of the individuals overwhelmingly responsible for the majority of per capita egg production per spawning event could be achieved by establishing minimum size limits of 30 cm LF for L. gibbus and P. indicus, and 45 cm LF for C. microrhinos. These minimum limits would also protect all immature individuals of L. gibbus and C. microrhinos (Fig.
Size class distribution of three exploited reef fishes from three market surveys in Fiji. A Lutjanus gibbus; B Parupeneus indicus; C Chlorurus microrhinos. Solid line = female L50; dashed line = male L50; dotted line = 90% cumulative per capita egg production. Note that x- and y-axis scales vary.
Our analyses of per capita egg production do not consider potential maternal effects, such as the possibility that larger females may spawn more often or produce higher quality eggs. Nor do they consider the typical population size structure of fishes, comprising many more small individuals than large individuals. The impact of the latter has been demonstrated by genetic parentage analysis showing that highly abundant mature fish contribute disproportionately to population replenishment (
We used rapid, histology-based methods to estimate Fiji-specific reproductive parameters for three reef fishes. We then used the parameter estimates to describe the reproductive characteristics of fish observed in Suva fish markets. The absence of females in the largest size classes of all three species suggests that, at the population level, individuals well below maximum size are responsible for the majority of egg production. Minimum size limits of 30 cm LF for Lutjanus gibbus and Parupeneus indicus, and 45 cm LF for Chlorurus microrhinos may enhance population-level egg production while also protecting almost all immature individuals of all three species.
The majority of the data upon which this study is based was produced by participants in a histology-training workshop: F. Aspestrand, D. Divalotu, K. Lavaki, A. McGregor, M. Peter, N. Qaqara, K. Samson, S. Singh, A. Soderberg, J. Tamanitoakula, T. Vodivodi, and P. Waqainabete. We thank W. Naisilisili and J. Tamanitoakula for logistical planning and support for, and Raina Hill-Lewenilovo and R. Rakesh for their assistance with, specimen collection. Financial support was provided by a grant from the National Geographic Society (NGS-154C-18). The Wildlife Conservation Society and the University of the South Pacific provided in-kind support. This is contribution 2022-002 to the Pacific Biological Survey, 1877 to the Hawaii Institute of Marine Biology, and 11 481 to the School of Ocean and Earth Science and Technology.