Research Article |
Corresponding author: Marcelo Reis ( marceloreis.bio@gmail.com ) Academic editor: Cassiano Monteiro-Neto
© 2020 Marcelo Reis, Will F. Figueira.
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:
Reis M, Figueira WF (2020) Age, growth and reproductive biology of two endemic demersal bycatch elasmobranchs: Trygonorrhina fasciata and Dentiraja australis (Chondrichthyes: Rhinopristiformes, Rajiformes) from Eastern Australia. Zoologia 37: 1-12. https://doi.org/10.3897/zoologia.37.e49318
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Bottom-dwelling elasmobranchs, such as guitarfishes, skates and stingrays are highly susceptible species to bycatch due to the overlap between their distribution and area of fishing operations. Catch data for this group is also often merged in generic categories preventing species-specific assessments. Along the east coast of Australia, the Eastern Fiddler Ray, Trygonorrhina fasciata (Muller & Henle, 1841), and the Sydney Skate, Dentiraja australis (Macleay, 1884), are common components of bycatch yet there is little information about their age, growth and reproductive timing, making impact assessment difficult. In this study the age and growth (from vertebral bands) as well as reproductive parameters of these two species are estimated and reported based on 171 specimens of Eastern Fiddler Rays (100 females and 71 males) and 81 Sydney Skates (47 females and 34 males). Based on von Bertalanffy growth curve fits, Eastern Fiddler Rays grew to larger sizes than Sydney Skate but did so more slowly (ray: L∞ = 109.61, t0 = 0.26 and K = 0.20; skate: L∞ = 51.95, t0 = -0.99 and K = 0.34 [both sexes combined]). Both species had higher liver weight ratios (HSI) during austral summer. Gonadal weight ratios (GSI) were higher in the austral winter for Eastern Fiddler and in the austral spring for Sydney Skates.
Age and growth, Rajidae, Rhinobatidae, sexual maturity
Demersal trawl fisheries have very high bycatch rates due to the low-selectivity of the gear. Very often, this bycatch includes species of bottom-dwelling elasmobranchs. There are very few directed elasmobranch fisheries worldwide (
Trygonorrhina fasciata
is a relatively common inshore batoid throughout its range (
Dentiraja australis
was once one of the most common skates on the continental shelf off Eastern Australia. However, evidence shows that it has declined significantly throughout its range. Fishery independent surveys off southern New South Wales (NSW) have shown that catch rates for “skates” combined have declined by 83% between 1976/1977 and 1996/1997 (
Information about life history traits is pivotal for fisheries management and conservation of any species. Elasmobranch management and conservation is frequently obstructed by the lack of knowledge at population levels (
Demersal elasmobranchs frequently are among the species with less information available, hindering further evaluation of stocks and restricting modelling of impacts. When such data are inadequate it is virtually impossible to assess population declines (
Samples were obtained by the Department of Primary Industries Fishery Observers program (DPI – Fisheries). Individuals were collected from October 2015 to December 2016; caught by commercial trawlers operating in the northern central coast of New South Wales (Fig.
Body measurements were made according to
The hepatosomatic index, which is the ratio of liver weight to total body weight (expressed as a percentage) and is used as an indicator of energy reserve, was calculated as: HSI = 100* (WL/W), where: WL = liver weight and W = total weight. Average values of HSI were calculated for combinations of sex and season (with exception of late austral summer and autumn months, due low number of samples) in order to identify periods of higher energy accumulation. Higher HSIs are normally found in periods preceding events of high metabolic activity such as migrations, reproduction, or cycles of low environmental productivity. Considering that neither of the species in this study is reported as migratory and both are endemic with relatively small distributions it is reasonable to assume that HSI seasonal changes will hinge mostly on reproduction cycles or seasonal oceanographic changes. Seasonal differences in average values of the Hepatosomatic Index between genders and species were tested through analysis of variance (two-way ANOVA) to test similarities of HSI values of males and females of both species on a seasonal basis.
A section of approximately 10 cm of the pre-caudal vertebrae for Eastern Fiddler Ray and 7.5 cm for Sydney Skates, consisting of approximately 8–10 vertebrae from the area above the pelvic girdle, was dissected from each specimen. The preparation of the vertebrae for enhancement, interpretation, and counting of growth rings was performed by washing with sodium hypochlorite (NaClO 0.05%) for 2–3 minutes and drying for 30 minutes at 60 °C before sectioning, following
Vertebral sections were examined for each set of wider opaque (calcified) and narrower translucent (less calcified) bands after the birth mark (Age 0) which was considered to be an individual growth band and represented the mark preceding one year of growth (Fig.
Photos of vertebrae section of Trygonorrhina fasciata (left, sampling code AP085 – 632 mm TL) and Dentiraja australis (right, sampling code 053 – 328 mm DW). White dots indicated by arrows show birth mark (BM), while the remaining highlight the growth opaque bands and the bar indicate vertebral radius (VR).
Two independent, non-consecutive ring counts were made by a single reader without knowledge of the specimen's ID, total length or disc width, previous counts, or sex. Final age estimates were assigned based on the agreement of two or more age readings. Reproducibility of the growth ring count was evaluated by age-bias plots and by the simple approach of calculating the percent reading agreement (PA = [No. agreed/No. read] x 100) within and between readings for all samples (
Growth curves were fit to size-at-age data using the von Bertalanffy growth model (
Marginal increment analysis (MIA) was used in order to determine the time of band formation (
Maturity stage of individuals was determined for females by macroscopic examination of the gonads following a modified version of previous studies (
In all, 171 specimens of T. fasciata (100 females and 71 males) and 81 D. australis (47 females and 34 males) were sampled. During the late austral summer and autumn months (January-May), sampling frequency was lower than expected, reflecting low catches of the species by the boats sampled for the observers' program. This prevented more conclusive results from reproductive data as well age validation through Marginal Increment Analysis (MIA). Nonetheless, patterns were observed and are described in more detail below.
Sampled Fiddler Rays ranged between 37.9 and 109.2 cm Lt (72.53 ± 15.5) and between 220 and 8900 g total weight while Sydney Skates ranged between 22.4 and 38.7 cm DW (32.5 ± 2.89) and 160 and 1064 g total weight. The relationship between Lt and DW were linear for both species. In Fiddler Rays the relationship was Lt = 0.44469DW + 0.13879 (r2 = 0.9184, p < 0.0001, n = 171, Fig.
There was no obvious difference in the nature of the length-weight relationships (using either DW or LT) of males vs females for either species though females tended to be bigger and heavier than males for both species, an effect that was more pronounced in T. fasciata (Figs
Vertebrae of 141 individuals of T. fasciata and 72 D. australis were sectioned and read. Vertebral growth-band readability of T. fasciata was higher (3.8 ± 0.03) than D. australis (2.2 ± 0.08). Sections considered unreadable accounted for 9.3% of the slides of T. fasciata (n = 16) and 10% of D. australis (n = 8) and hence were excluded from any further analysis. Repeated age estimates agreed closely and there was no systematic bias between readings for either species. The percentage of reading agreement (PA) for T. fasciata was 95.74% and for D. australis was of 94.44%. There were significant linear relationships between the radius of pre-caudal vertebrae and total length for both species, indicating that these vertebrae were suitable structures for age determination (Table
Linear relationship parameters between vertebral radius and species total length for Trygonorrhina fasciata and Dentiraja australis. Values of parameters for the equation TL = a+b*VR, where: (VR) vertebral radius, (TL) animal total length, (a) slope, (b) intercept, (n) sample size, (r2) square of regression correlation coefficient; and p is the probability of statistical significance.
Species | a (± SE) | b (± SE) | n | r2 | p |
T. fasciata | 30.79 (0.73) | 15.74 (0.30) | 141 | 0.96 | < 0.0001 |
D. australis | 10.13 (0.91) | 24.07 (2.65) | 72 | 0.67 | < 0.0001 |
The oldest estimated age for a male of T. fasciata in this study was 10 years (Lt = 76.6 cm) whereas the largest male (Lt = 88.2cm) was estimated to be seven years old. The estimated age of the oldest female for the species was 15 years (Lt = 109.5cm) which was also the largest female. Among samples of D. australis the oldest male was estimated to be seven years old (TL = 48.7cm) while the largest male (TL = 50.8cm) was estimated to be 6 years old. The oldest female D. australis was also the largest with age estimated to be seven years (TL = 51.9cm). The growth curve for T. fasciata was described by the VBGM as L∞ = 109.61, t0 = 0.26 and K = 0.20 whereas the D. australis was L∞ = 51.95, t0 = -0.99 and K = 0.34 (Figs
Summary of fitted parameter values and results for Trygonorrhina fasciata and Dentiraja australis. In parentheses are the upper and lower bounds of the 95% confidence intervals for each of the parameters.
Species | Asymptotic length (L∞) | Growth curvature K | t0 | n |
T. fasciata | 109.61 (108.9, 115.1) | 0.20 (0.12, 0.23) | 0.26 | 141 |
D. australis | 51.95 (51.90, 53.45) | 0.34 (0.06, 0.44) | -0.99 | 72 |
The vertebral marginal increments for T. fasciata were highest in July, corresponding to mid austral winter (Fig.
There were a limited number of samples available from January to May 2016 (late austral summer and autumn) for both species (n = 5, 3 T. fasciata, 2 D. australis). This was also the case for samples of D. australis in late winter and early spring, specifically between August and October, where only six individuals were caught (2 females and 4 males). These low numbers prevented a comprehensive evaluation of reproductive capacity throughout the year.
Results of the two-way analysis of variance comparing the seasonal average values of the Hepatosomatic Index (HSI) of T. fasciata indicated that seasons have a statistically significant effect (p < 0.05) (Table
Hepatosomatic index (13–15) and gonadosomatic index (16–18) with standard error (±2 SE) for sampled specimens of Trygonorrhina fasciata. Results of HSI considering both sexes (13), females only (14) and males only (15) and GSI considering both sexes (16), females only (17) and males only (18).
Summary of results of the two-way analysis of variance for the Hepatosomatic Index (HSI) and the gonadosomatic index (GSI) of sampled specimens of Trygonorrhina fasciata and Dentiraja australis. Significant results are marked with (*).
Index | Trygonorrhina fasciata | Dentiraja australis | ||||||||||
Sum of sqrs | d.f. | Mean square | F | p | Sum of sqrs | d.f. | Mean square | F | p (same) | |||
HSI | Sex | 3.330 | 1 | 3.330 | 1.116 | 0.292 | 9.174 | 1 | 9.174 | 8.209 | 0.005* | |
Season | 21.288 | 2 | 10.644 | 3.567 | 0.030* | 4.684 | 2 | 2.342 | 2.096 | 0.13 | ||
Sex*Season | 5.270 | 2 | 2.635 | 0.883 | 0.415 | 0.67 | 2 | 0.335 | 0.3 | 0.741 | ||
Within | 417.798 | 140 | 2.984 | 82.703 | 74 | 1.117 | ||||||
Total | 446.918 | 145 | 95.851 | 79 | ||||||||
GSI | Sex | 0.911 | 1 | 0.911 | 6.27 | 0.013* | 61.617 | 1 | 61.617 | 35.54 | < 0.001* | |
Season | 0.462 | 2 | 0.231 | 1.59 | 0.207 | 6.32 | 2 | 3.16 | 1.823 | 0.168 | ||
Sex*Season | 0.051 | 2 | 0.025 | 0.176 | 0.838 | 4.953 | 2 | 2.476 | 1.429 | 0.246 | ||
Within | 20.358 | 140 | 0.145 | 128.292 | 74 | 1.733 | ||||||
Total | 21.789 | 145 | 200.358 | 79 |
Analysis of variance of the average Hepatosomatic Index (HSI) and Gonadosomatic Index (GSI) of sampled D. australis indicated a statistically significant effect of gender but not of seasons or in the interaction between these factors (Table
The highest ratios of maturing and more importantly, of pregnant females for T. fasciata were found in late austral spring and early summer, indicating that the austral summer might be the period likely to be related to reproduction (Table
Hepatosomatic index (19–21) and gonadosomatic index (22–24) with standard error (±2 SE) for sampled specimens of Dentiraja australis. Results of HSI considering both sexes (19), females only (20) and males only (21) and GSI considering both sexes (22), females only (23) and males only (24).
This study presents the partial estimations of age, growth and reproductive biology of two endemic demersal elasmobranchs of the Australian East Coast: T. fasciata and D. australis. The distribution patterns of these species and of fishing operations suggest a high probability of bycatch in demersal trawl and gillnet fishing, which combined, comprise the majority (94.75%) of the commercial fishing operations in the East Coast (
Despite similar distributions and generalized descriptive classification as batoids, direct morphometric and ontogenetic comparisons between the T. fasciata and D. australis are not plausible due to distinct features of both species. Nonetheless, the estimated growth rate of T. fasciata seems to be slower than those derived for D. australis. The Von Bertalanffy growth curve of T. fasciata suggested that bigger and therefore older individuals may not have been caught by the sampling. Perhaps these larger specimens inhabit deeper waters not exploited by the fishery. Similarly, due the relatively small sizes of D. australis, potentially smaller individuals were not caught due to mesh size.
The estimated growth rates of D. australis were relatively fast for an elasmobranch, even considering its small size. Almost all elasmobranch species have slower growth rates, with curvature parameters (Von Bertalanffy k) ranging normally from 0.05 to 0.25 (
It should be noted that these age estimates are preliminary since this study has not explicitly validated the annual nature of the rings. This was partly due to the lack of sufficient samples from all months of the year, especially for D. australis. However, there was also a considerable variation in the marginal increment data. There was a relatively pronounced drop in the distance around October for T. fasciata suggesting this as the time of band formation. There is insufficient data to determine the same for D. australis. Nonetheless, from this low value, we did not see the expected steadily increasing increment width. It is possible this is due to measurement error caused by the lack of a defined border between the dark and light portions of the banding pattern. Despite this variance, vertebral radius was determined to be an appropriate ageing structure based on the positive linear relationship between vertebrae radius and total length. Thus while annual vertebral growth bands are quite common in other similar species (
Gonadosomatic Index results presented in this study suggest T. fasciata are reproducing in late austral winter/early spring whilst D. australis might be reproducing in late austral spring and summer. This assumption is supported by HSI results since both species had overall smaller averages during austral winter months and presented increasing values towards summer. Similar to related species at the same latitudes, HSI's of females may not show significant differences during egg growth because lipids and proteins may be stored and processed continuously throughout seasons without significant changes in biomass (
One of the biggest concerns to managers when assessing stocks of Elasmobranch bycatch is the uncertainty caused by the rarely differentiated species in landings information (
This study provides basic information about growth and reproduction of two endemic Australian species: T. fasciata and D. australis that like many other species of elasmobranchs, require species-directed management actions, especially considering the high susceptibility of these and many other demersal species to fishing bycatch and direct consequences such as overexploitation. The latter is a particularly serious problem to elasmobranchs because, compared to other marine fishes, the group have relatively low productivity and therefore differ from other fish in their ability to withstand and recover from exploitation (
The authors would like to thank Daniel Johnson, Matt Harrison and Vic Peddemors and the Department of Primary Industries – Fisheries Observers Program for the samples provided for this study, the Sydney Institute of Marine Sciences (SIMS) for the use of facilities, Mark Macinante for the assistance with dissections and to the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior for scholarship funding (Process BEX 13590-13-8). This research was conducted under animal ethics approval (ACEC ref: 16/02) to the NSW Department of Primary Industries. This is contribution 263 to the Sydney Institute of Marine Science. The authors are responsible for the content, including any improprieties in use of the English language.