let o fl ^ilasiopli^ · brothers jirif %han, 94usadiq (rafiq, musashir shamim, (dr. owais yaqoot...

r PRECISION OF HARD STRUCTURES US ESTIMATE AGE AND GROWTH OF SL

FRESHWATER TELEOST

DISSERTATION

SUBMITTED IN PARTIAL FULFILMENT OF THE R FOk THE AWARD OF THE DEGREE OF

le t ol f ilasiopli '•f-.

'•H^ ^^>^ 3n f-1

\ ^

SABAH ^jf'

UnderIhe Supervisior

DR. MOHAMMAD AFZAL KHAN

FE SCIEN MUNIVEh

£.\f i ^

3 0 JAN 20i5

DS4408

'SaM/f

Phone< External: 2700920/21-3430 Internal : 3430, 3431

DEPARTMENT OF ZOOLOGY ALIGARH MUSLIM UNIVERSITY

ALIGARH - 202 002 INDIA

Sections: 1. ENTOMOLOGY , er^FISHERY SCIENCE & AQUACULTURE 3. GENETICS 4. NEMATOLOGY i P - /^U 1 ^ 5. PARASITOLOGY Dated. \9. ftH". )...T^.,

D. No /ZD

CERTIFICATE

This is to certify that the dissertation entitled "Precision of hard structures used to

estimate age and growth of selected freshwater teleost" has been completed under/ :" >; f . I ' . , , •

my supervision by Ms. Sabah. The work is original and independently pursued by the

candidate. It embodies some interesting observations contributing to the existing ' >i,

knowledge on the subject.

I permit the candidate to submit the dissertation work for the award of M. Phil.

Degree in Zoology.

riiv ^^'^ (Dr. Mohammad Afzal Khan)

Assistant Professor

JicôwCecfgement

I cypress my sincere gratitude to J^CmigHty Mlafi who Ras given me strength to complete

tfiis worH^successfufCy and produce in its present form.

It is my priviCege and gives me immense pleasure to express sound perception of

gratitude to my Supervisor <Dr. Mohammad^fzal%jian for fiis continuous encouragement,

vafuaSCe and constructive suggestions. 'Wor^ng under his guidance is a matter of great

privifege.

I extend my thanlis and gratitude to (prof. Iifan ^hmad, Charrmait of the

(Department ofZoofogy, Jl.M.'V, for providing aCC necessary faciCities reiatedto my work^

I wouldatso [ike to thanh^<PTof. IqSaCâfvez, <Prof. Mu^tar_^hmad%han and

(Dr. SaCtanat (Parveenfor their vafuaBfe advice.

Special thanlis are also due for my seniors (Dr. Jiagma, !Mr %aish 'Miyan, iM.s.

Shahista 'Kfian, coffeagues Safman Kfian and_Afaq [Hazir Shah and to my friends Sumu\d

JAhad, J4rjumend Shaheen, !Kida %iâni, Saima hameed, SharSa %ausar, Sayma Samreen.

SyedSuraya, (pyiiqaui TaSasum, îaffia 'Mustahj-m, Dania j^hmed, (Riishda Sharaf, 'Taihd

Saeed, Tarzana Imtiaz, Vzm.a Vsmain, Jlh. Latif 'Wain, !M. (Farced, Sajad (Bhat and

(prince Tariquefor their unconditional and constant help.

I am extremely proud to achjiowledge the contriSution of my family especially Dr.

Ahdul (p^sliidSheilfi, Kilal 9dali({^ Javaid Malil{, (RuSina 9dalih^ Pûhi'Malih^ C'handi

Mushtaq and (Dr. 'Mushtaq Wani and, sisters Shiraza Wani, Jdaadi !Mir, 9Audasir (Rgfiq,

(Dr <Enas Mushtaq, Jdafsa Maliki (Rayeesa Maliî Madhiya 'Malih^ and yfuha 'Malif^

Brothers Jirif %han, 94usadiq (Rafiq, MuSashir Shamim, Yaqoot (Bhat, (Dr. Owais

Mushtaq, JLthar Malill and (Riyaza 'Wani Last, hut not the least, I am privileged to

express my deepest thanlis to the most precious gift of god, my loving parents and

grandparents for Being a source of unseen. But not unheard strength that installed courage

in me to complete this worh^

(SaBah)

CONTENTS

Particulars Page no.

INTRODUCTION 1-8

A SHORT DESCRIPTION OF FISHES 9-14

MATERIALS AND METHODS 15-20

RESULTS 21-25

DISCUSSION 26-33

SUMMARY 34

REFERENCES 35-53

APPENDIX

LIST OF TABLES

No. Title

1 Comparison of percent agreement (PA), average percent error (APE) and

coefficient of variation (CV) between the age readings of two independent readers

in Schizopyge cunnfrons, Schizopyge niger and Schizothorax esocinus.

2 Comparison of percent agreement (PA), average percent error (APE) and

coefficient of variation (CV) among ages assigned between structures iii

Schizopyge cunifrons, Schizopyge niger and Schizothorax esocinus.

3 Comparison of Pearson's correlation coefficient values in Schizopyge cuni/rons.

Schizopyge niger and Schizothorax esocinus.

4 Comparison of mean values of age estimates from different bony parts in

Schizopyge ciirvifrons, Schizopyge niger and Schizothorax esocinus.

5 von Bertalanffy growth parameters along with growth perfomiance index ( o ) in

Schizopyge curvif'rons, Schizopyge niger and Schizothoixix esocinus.

6 Estimated parameters of length-weight relationship (LWR) for Schizopvgc

curvifrons, Schizopyge niger and Schizothorax esocinus.

7 Length-length relationships (LLRs) between total length (TL), fork length (PL)

and standard length (SL) for Schizopyge curvifrons, Schizopyge niger and

Schizothorax esocinus.

LIST OF FIGURES

No. Title

1 Age bias plots for age comparisons between readers for scales, opercular

bones, otoliths, vertebrae and cleithra in Schizopyge cunifrons.

2 Age bias plots for age comparisons between readers for scales, opercular

bones, otoliths, vertebrae and cleithra in Schizopyge nigcr.

^ Age bias plots for age comparisons between readers for scales, opercular

bones, otoliths, vertebrae and cleithra in Schizothorax esocinus.

4 Age bias graphs for age comparisons between structures in Schizopyge

curvifrons.

5 Age bias graphs for age comparisons between structures in Schizopyge nigcr.

6 Age bias graphs for age comparisons between structures in Schizothorax

esocinus.

7 von Bertalanffy growth curves for Schizopyge curvifrons, Schizopyge niger

and Schizothorax esocinus showing back-calculated length at estimated age.

INTRODUCTION

Fishes are considered to be an excellent source of high quality protein, other essential

nutrients and minerals that are often difficult to obtain from many other sources. As

per FAO reports (2012), fish is the most valuable agricultural commodity traded

intemafionally with annual sales of nearly US$217.5 billion in the year 2010 and

increasing each year. Fisheries and aquaculture provided livelihoods and income for

an estimated 54.8 million people engaged in the primary sector of fish production in

2010, of which an estimated 7 million were occasional fishers and fish fanners. Asia

accounts for more than 87 percent of the world total followed by Africa (more than 7

percent), and Latin America and the Caribbean (3.6 percent). Capture fisheries and

aquaculture supplied the world with about 148 million tons offish in 2010. In 2009.

fish accounted for 16.6 percent of the global population's intake of animal protein and

6.5 percent of all protein consumed. Inland fisheries are a vital component in the

livelihoods of people in many parts of the world, in both developing and developed

countries. Total global inland capture fisheries production has increased dramatically

since the mid-2000s with reported (as submitted by countries) and estimated (by FAO

in cases of non-reporting countries) total production at 11.2 million tonnes in 2010, an

increase of 30 percent since 2004. Growth in the global fish calch from inland waters

is wholly attributable to Asian countries. With the remarkable increases reported for

2010 production by India, China and Myanmar, Asia's share is approaching 70

percent of global production (FAO, 2012).

The growth in fish catch from inland waters is also accompanied by drastic

decline in the number of several commercially important fish species from natural

environment. Inland waters are considered as being overfished in many parts of the

world, and human pressure and changes in the environmental condifions have

seriously degraded important bodies of freshwater (FAO, 2012). Freshwater fishes in

India are under threat for several reasons, but primarily due to unsustainable and

unethical fishing practices. Though there are only a few species of fishes that are in

trade, the state of all fi-eshwater fishes in India is in danger because of wrongful

methods of fishing. Other common threats that affect freshwater fish populations are

habitat loss due to dredging of lakes and rivers, filling, altering river courses, dams,

irrigation canals, and other reasons. Of the three species selected for the study, two

1

species are listed Vulnerable {Schizopyge curvifrons and Schizopyge niger) and one as

Lower risk-near threatened (Schizothorax esocinus) (Molur and Walker, 1998).

Studies on biological parameters of threatened fishes are highly significant for

management and conservation of populations in natural water bodies (Sarkar et al.,

2009; Hossain et al., 2012; Khan et al., 2012b).

India is one of the richest countries in terms of freshwater resources. India has

vast freshwater resources in the form of ponds, tanks, lakes, reservoirs, rivers, bheels,

canals, swamps, marshes, etc. Ponds and tanks account for about 2.25 million ha.

Lakes comprise 26 million ha, while reservoirs (major and medium) have spread over

an area of 3.0 million ha.'Rivers have a total length of more than 27,000 km. Canals

and channels and their network run up to 112,000 km. Bheels (water bodies fonned

due to the serpentine course of a flooded river), marshes and swamps constitute 7.9

million ha (Basavaraja, 2007). The water resources of Kashmir can be broadly divided

into lotic and lentic systems. The fomier comprises of the river Jhelum and various

streams which directly or indirectly join it, while the latter includes lakes, ponds,

wetlands and other similar aquatic habitats. River Jhelum flows from south to north

west up to Wular, from where it takes south westerly direction. The total length of the

river from the Veerinag up to Uri is about 239 km. There are a number of mountain-

and valley-lakes in Kashmir. Some of these are Dal, Anchar, Manasbal, Gangabal,

Wular lakes. The variety of ton-ential hill streams, rivers and lakes support good fish

diversity. These aquatic resources have been meeting the requirement of fishes for the

local people over the time immemorial. Over the years various changes have taken

place in the species composition, distribution and availability of fishes in the water

bodies of this region. The streams and lakes of the valley harbour a number of

indigenous fishes belonging to genus Schizothorax, Schizopyge, and other carps that

serve as an important food item for human consumption.

Studies on fish biology particularly morphometry, length-weight relationship,

condition factor, reproduction, food and feeding habit, etc. are important not only to

provide additional information to the existing knowledge but also in the utility of the

knowledge in increasing the technological efficiencies of the fishery entrepreneurs for

evolving judicious fisheries and aquaculture management. Age and growth analyses

of fish species are used to deteimine longevity, mortality, productivity, yield and

population dynamics, which in turn are essential for responsible management

(Holden, 1972; Hale and Lowe, 2008). Age estimation in fishes have been undertaken

using different hard structures such as, scales (Singh and Shamia, 1995; Andreu-Soler

et al., 2003; Aydin et al , 2003; Dua and Kumar, 2006; Karatas et al, 2007; Zhang

and Takita, 2007; Sarkar et al., 2008; Ozcan and Bahk, 2009; Ujjania, 2012), fin rays

and spines (Ezenwa and Ikusemiju, 1981; Morrow Jr. et al., 1998; Stevenson and

Secor, 1999; Kano, 2000; Sun et al., 2002; Mills and Chalanchuk, 2004; Penha et al,

2004; Whiteman et al., 2004; Metcalf and Swearer, 2005; Santamaria et al., 2009;

Tribuzio et al., 2010), otoliths (Doray et al., 2004; Monteiro et al., 2006; Qiu and

Chen, 2009; Ilkyaz et al, 2010; Ma et al., 2010; Jia and Chen, 2011; Huo et al., 2012).

opercular bones (Bardach, 1955; Qasim and Bhatt, 1964; Jellyman, 1980; Nargis.

2006; Gomez-Marquez et al, 2008), vertebrae (Guinn and Hallberg, 1990; Polat et al.

2001; Coelho and Erzini, 2002; Licandeo et al, 2006; Hale and Lowe, 2008; Kume et

al, 2008), cleithra (Govind and Gopal, 1966; Harrison and Hadley, 1979; Casselman,

1990) and some other bony parts. Scales have been widely used for ageing because

they are collected, prepared and read easily (Gursoy et al, 2005). However, several

researchers have reported that scales can provide unreliable estimates of fish age

(DeVries and Frie 1996; Maceina and Sammons, 2006), which has often been

attributed to reabsorption and deposition of false annuh due to stress and food

limitation and also because clarity of annuli is affected with increase in fish age (Khan

et al, 2011a) and have, therefore forced fishery scientists to use other calcified

stiTictures (Hammers and Miranda, 1991; Zoubi, et al, 2010). It is now well

established that a suitable structure for age estimation \'aries by species and

geographic location (Koch et al, 2009), thus the evaluation of the precision and

accuracy of bony structures should be studied (Polat et al, 2001). Precision is defined

as the reproducibility of repeated measurements on a given structure or the

repeatability of individual readings or age estimates, whether or not those

measurements (age readings) are accurate. It is not unusual for inaccurate age

readings to be highly reproducible (in other words, precisely wrong) or to show no

relationship between accuracy and precision (Campana et al, 1990; Campana and

Moksness, 1991; Campana, 1995). Therefore, precision cannot be used as a proxy for

accuracy. Nevertheless, a measure of precision is a valuable means of assessing the

relative ease of determining the age of a particular structure, of assessing the

reproducibility of an individual's age determinafions, or of comparing the skill level

of one ager relative to that of others (Campana, 2001). However, higher precision of

age estimates provides no insight into the biases or accuracy of age estimates among

or between structures. The application of a validation method is required for accurate

age estimations (Beamish and McFarlane, 1983), but the method of counting annuli in

hard structures and measuring the level of precision between structures and between

researchers is the best way to corroborate age estimations if a method of validation

cannot be established (Kimura et al., 2006; Gumus et al., 2010). Counting growth

increments (annuli) on otoliths, scales or other hard structures has been the most

common method for ageing fish; however, age estimation is often accompanied by

several sources of error that can have significant effects on many population

parameter estimates (Beamish and McFarlane, 1983) e.g., age underestimation may

result in optimistic estimates of growth and mortality rates, leading to the serious

overexploitation of the population and its eventual collapse (Campana, 2001).

Comparison of age estimates from various bony structures has been reported in a

number of fishes to identify the most suitable structure for a fish population (Gocer

and Ekingen, 2005; Sylvester and Berry, 2006; Jackson et al., 2007; Phelps et al.,

2007; Khan and Khan, 2009; Khan et al, 201 la, b; Ma et al, 2011).

However, there are no published reports available on precision of different

structures for ageing fishes selected for the present study {Schizopyge curvifrons,

Schizopyge niger and Schizothorax esocinus).

Age and growth are always used together in phraseology, but each terni has its

own distinct meaning, which, as cited by Goldman (2004), was eloquently stated by

DeVries and Erie (1996): "Age refers to some quantitative description of the length of

time that an organism has lived, whereas growth is the change in body or body part

size between two points in time, and growth rate is a measure of change in some

metric of fish size as a fimction of fime". Growth is one of the most important life

history processes influencing the fish population dynamics (Zhan, 1995). For a given

fish species, reliable estimation of growth is critical in developing sustainable

fisheries stock assessment and management (King, 1995; Gang et al, 2008). The main

objective of age and growth studies in fish is to estimate their mean size at each age

class and determine their growth parameters (Mather et al, 1995; Santamaria et al,

2009). Estimates of growth drive size- and age-structured stock assessment models

(Quinn and Deriso, 1999), scale yield calculations (Beverton and Holt, 1957; Gulland,

1983; Haddon, 2001) and are related to life history traits such as natural mortality and

4

age or length at maturity (Chamov, 1993; Jensen, 1998). Besides pure application, age

and growth studies are also important in describing the basic biology and ecology of

fishes (Weatherley and Gill, 1987; Cailliet and Goldman, 2004; Cope and Punt,

2007). Growth rate estimated trom length-at-age data are considered to assess fish

stocks with relatively higher accuracy than the method based on length- frequency

data. Fish growth data can be easily fitted with an appropriate mathematical fiinction

to generalize the growth process, so as to predict the growth trend and compare the

growth patterns among stocks or species (Rao, 1958; Gang et al., 2008). Several

mathematical models can be used for modelling fish growth, however, the von

Bertalanffy growth function (VBGF; von Bertalanffy, 1938) is by far the most studied

and most widely used of all length-age models in fisheries, and its parameters are

particularly useful in describing general fish growth (Chen et al., 1992; Quinn and

Deriso, 1999), deriving fisheries reference points (Clark, 1991; Williams and

Shertzer, 2003) and estimating life history parameters (Beverton and Holt, 1959;

Beverton, 1992; Cope and Punt, 2007). Since the incepfion of the VBGF, there has

been a steady evolufion in its use and estimation. Beverton and Holt (1957)

popularized the current form of the VBGF by changing the original three-parameter

fonnulation to include to rather than Lo. Several estimation techniques, ranging from

linear fitting (Walford, 1946; Stamatopoulos and Caddy, 1989) to nonlinear least

squares (Tomlinson and Abramson, 1961; Marquardt, 1963), iterative fitting (Rafail,

1973), and likelihood (Kimura, 1980) methods have subsequently been proposed

(Cope and Punt, 2007).

The growth rate of fish is an essential component of models used in stock

assessment offish populations; small variations in growth rates can have a significant

impact on modelling outcomes for populafion analysis (Megalofonou, 2000;

Santamaria et al., 2009).

Age and growth have been studied in a number of fishes from India such as

Cirrhinus mrigala (Ham.) from the river Ganga (Jhingran, 1959); Ophicephalus

punctatus Bloch from ponds in Aligarh (Qasim and Bhatt, 1966); Labeo rohita

(Ham.) from a pond (Moat) and rivers Ganga and Yamuna (Khan and Siddiqui,

1973); three Indian major carps from Hirakud reservoir (Mathew and Zacharia,

1982); Tachysurus dussu,nieri (Val.) along the Dakshina Kannada Coast

(Vasudevappa and James, 1988); Indian major Carp {Catla catla Ham. 1822) from

northern India (Johal and Tandon, 1992) and from selected water bodies of southern

Rajasthan (Ujjania, 2012); Johnieops sina (Pisces/Percifonnes) from Bombay

waters (Chakraborty, 1994); threadfm bream Nemipterus japonicas (Bloch) off

Bombay (Chakraborty, 1995); Channa marulius from Harike wetland (A Ramsar

site), Punjab (Dua and Kumar, 2006); Turbo brunneus occurring in Tuticorin coastal

waters (Ramesh et al., 2009); Sillago sihama (Forsskal) from Zuari estuary, Goa

(Shamsan and Ansari, 2010); silverbellies along Kerala coast (Abraham et al., 2011)

and Thunnus albacares (Bonnaterre, 1788) (Rohit et al., 2012). There have been few

studies on the age and growth of fishes belonging to sub-family Schizothoracinae viz.

Schizothorax richardsonii from the Garhwal hills, India (Singh and Shamia, 1995),

Schizopygopsis yoimghiisbandi younghiisbandi (Chen et al., 2009), Ptychobarbiis

dipogon (Regan, 1905) (Li and Chen, 2009), Schizothorax waltoni (Qiu and Chen,

2009); Schizothorax o'connori (Yao et al, 2009; Ma et al., 2010), and

Oxygymnocypris stewartii (Jia and Chen, 2011; Huo et al., 2012) in the Yarlung

Tsangpo river, Tibet. Despite the limited distribution of 5. curvifrons, S. niger and S.

esocinus and their importance to fishing, little is known about its biology and ecology.

Sunder and Subla (1984) demonstrated age and growth of Schizothorax cunnfrons by

back-calculation.

Fisheries management and research often requires the use of biometric

relationships in order to transfomi data collected in the field into appropriate indices

(Anderson and Gutreuter, 1983; Ecoutin and Albaret, 2003; Mendes et al., 2004). One

of the most extensively used in any analysis of fishery data is the length- weight

relationship (LWR). Furthennore, Length-weight relationship allows; i) estimation of

average weight of the fish of a given length group (Beyer, 1987); ii) conversion of

growth-in-length equations to growth-in-weight in order to estimate stock biomass

from limited sample size (Tarkan et al., 2009); iii) interspecific and inter populafional

morphometric comparison of fish species (Rajkumar et al., 2006); iv) study of the

ontogenic allometric changes in fish growth (Teixeira-de Mello et al., 2006) and v)

possible effects from parasites (Teixeira-de Mello and Eguren, 2008; Teixeira-de

Mello et al., 2011). Besides this, LWR can also be used in setting yield equations for

estimating the number of fish landed and comparing the population in space and time

(Beverton and Holt, 1957) and in frophic studies (Gonzalez-Gandara et al. 2003;

Sivashanthini, 2008). LWR parameters may change in relation to sex, body size,

6

temporal and / or spatial factors but variations of population structure, food

availability and fishing pressure can also result in different weight-length

relationships for the very same species (Giacalone et al., 2010). Knowledge on LWR

and length- length relationships (LLR) is useful in fish stock and population

assessments (Ricker, 1968). LLRs are important for comparative growth studies

(Moutopoulos and Stergiou, 2002; Hossain et al., 2006). Size conversions (e.g.,

calculated TL from SL) find applied value in fisheries for understanding several

aspects of population dynamics (Froese and Pauly, 2005; Ruiz-Campos et al., 2006).

Length and weight measurements in combination with age data can give

infonnation on the stock composition, age at maturity, life span, mortality,

growth and production (Beyer, 1987; Bolger and Connoly, 1989; King, 1996a, b; Diaz

et. al., 2000; Fafioye and Oluajo, 2005).

Condition factor is a quantitative parameter of the state of well-being of the

fish that will detemiine present and future population success by its influence on

growth, reproduction and survival (Hossain et al., 2006). Fulton's condition factor (K)

is widely used in fisheries and fish biology studies to describe a two-dimensional

weight-length relationship by converting it into a single statistic with the intention

describing the "condition" of that individual fish (Amason et al., 2009). The condition

of a fish reflects recent physical and biological circumstances, and fluctuates by

interaction among feeding conditions, parasitic infections and physiological factors

(Le Cren, 1951; Hossain et al., 2006). Condition factor is also a useful index for

monitoring feeding intensity, age, and growth rates in fish (Oni et al., 1983; Kumolu-

.Johnson and Ndimele, 2010).

LWR have been extensively studied in a number of fish species such as

Cyprinus carpio communis and Ctenopharyngodon idella from Himachal Pradesh

(Dhanze and Dhanze, 1997); Horabagrus brachysoma (Gunther) from Kerala (Kumar

et al., 1999; Anvar et al., 2008); Channa punctata (Bloch, 1793) from Western Ghats

rivers of Tamil Nadu (Haniffa et al., 2006); Rasbora daniconius (Hamilton-

Buchanan) from Sharavathi reservoir, Kamataka (Kumar et al., 2006); Puntius

filamentosus from Chalakudy river, Kerala (Prasad and Ali, 2007); Chiiala chitala

(Hamilton 1822) from the river Ganga basin, India (Sarkar et al., 2009); Tor putitora

(Hamilton, 1822) from the Ladhiya river, Uttarakhand (Pafiyal et al., 2010); fourteen

freshwater fish species from the Betwa (Yamuna river tributary) and Gomti (Ganga

7

river tributary) rivers (Sani et al., 2010); nine freshwater teleosts belonging to families

Clariidae, Channidae, Cyprinidae, Siluridae, Sisoridae and Bagridae collected from

river Ganga (Khan et al., 2011c); fourteen species belonging lo families Cyprinidae,

Bagridae, Siluridae and Pangasidae from Cauvery river at Hogenakal in south India

(Muralidharan et al., 2011) and Channa marulius and Heteropneustes fossilis form the

river Ganga (Khan et al., 2012a). LWR and LLR have been studied in Labeo bata,

Channa punctata, Ompok pabda and Mastacembelus armatus from river Ganga

(Khan et al, 2012b). Saha et al. (2009) studied LWR and condition factor in Thenus

orientalis (Lund, 1793) along East Coast of India. Gupta et al. (2011) studied the

LWR, LLR and condition factor in Ompok pabda (Hamilton 1822) (Silurifomies:

Siluridae) from the river Gomti, a tributary of the river Ganga. However, studies on

length-weight relationships for fresh water fish resources of Kashmir are scarce. Some

of the contributions available are: LWR and condition factor oi' Schizopyge curvifrons

from river Jhelum (Mir et al., 2012), Schizopyge esocinus from Kashmir waters

(Bhagat and Sunder, 1984; Dar et al., 2012), Scizopyge nlger from Dal lake (Shafi and

Yousuf, 2012); LWR of 5. plagiostomus, S. esocinus and S. labiatus from river Lidder

(Bhat et al. , 2010) and LWR and LLR for two species oi Schizopyge (S. curvifrons

and S. niger) and three species of Schizothorax {S. esocinus, S. labiatus and S.

plagiostomus) from the Kashmir valley of India (Khan and Sabah, 2013; fomis part of

this dissertation).

A critical appraisal of the available literature, as discussed above, warranted

the need to generate the basic biological information on the selected fish species from

Kashmir valley. In an attempt to respond to such a need, the present study was

undertaken with the following objectives:

1. to evaluate and compare age estimates, and reader precision between

different structures (i.e. scales, opercular bones, otoliths, vertebrae and

cleithra) for age determination of Schizopyge curvifrons, Schizopyge niger

and Schizothorax esocinus.

2. to fit the length-at-age data to the von Bertalanffy growth model, and

3. to investigate the length-weight, length-length relationship and condition

factor for all the three fish species.

/ i

^ short description

ofjlshes

Schizopyge curvifrons (Heckel, 1838)

Kingdom Animalia

Phylum Chordata

Subphylum Vertebrata

Superclass Pisces

Class Osteichthyes

Subclass Actinopterygii

Subdivision Teleostei

Order Cypriniformes

Family Cyprinidae

Subfamily Schizothoracinae

Genus Schizopyge

Species curvifrons

Schizopyge curvifrons (Heckel, 1838)

Common names

Sattar snowtrout English

S attar Kashmiri

Salient features

Body is elongate, ftisiform with a short, blunt and slightly prognathous upper jaw. S.

curvifrons differs from all other Kashmir valley Schizothoracinae fishes in having

more gill rakers (21-28) and in the thin lips, without enlarged lateral or median flaps

or the fleshy appearance. Scales are very small; lateral line with 95 to 121 scales.

Scales on anal sheath slightly larger than body scales (Kullander et al., 1999).

Colour: light brownish, belly silvery.

Geographical distribution

Asia: Afghanistan, Pakistan, India (Menon, 1999) and China (Walker and Yang,

1999). Reported from Iran (Coad, 1995), Uzbekistan (Kamilov and Urchinov, 1995),

Kazakhstan and Kyrgyzstan (Berg, 1964) (FishBase, 2012).

Fishery information

S. curvifrons is a good prized indigenous herbivorous cold freshwater teleost of

Kashmir Valley (Mir et al., 2012). This large-sized species attains a maximum length

of 40 cm (TL) and maximum weight of 1.25 kg (Talwar and Jhingran, 1991). This

species inhabits river, lakes and swamps. Mature adults undertake spawning migration

to incoming streams and breeding takes place amidst gravel and sandy beds (Raina

and Petr, 1999). Spawning period is extremely protracted, from May until the

beginning of August. Large specimens spawn earlier than the small ones (FishBase,

2012).

Schizopyge niger (Meckel, 1838)

Kingdom Animalia

Phylum Chordata


Superclass Pisces

Class Osteichthyes



Order Cypriniformes

Family Cyprinidae


Genus Schizopyge

Species niger

Schizopyge niger (Heckel, 1838)

Common names

Alghad snowtrout English

Ale gaad Kashmiri

Salient features

Body is elongate, fiasiform, with a short, blunt and slightly prognathous upper jaw.

Lips thick but not expanded into wide folds. Barbels two pairs (maxillary and

mandibular). A series of enlarged scales are present along the anal-fin base. Scales are

very small, 92 to 100 in the lateral line (Kullander et al., 1999).

Colour

The fish is much darker in colour than other species of the genus.


Asia: Kashmir Valley in India. Inhabits lakes and adjoining channels (Talwar and

Jhingran, 1991).

Fishery information

This species attains a maximum length of 27.0 cm (SL) (Kullander, 1999) and

maximum weight of 2.7 kg (Talwar and .Thingran, 1991). S. niger doesn't normally

occur in running water and is chiefly found in lakes (Kullander et al., 1999). It feeds

on detritus. Breeding grounds are found in shallow parts of lakes, particularly on the

roots of willow trees (Raina and Petr, 1999; FishBase, 2012). S. niger being a truly

lacustrine fish does not show any spawning migration (Shafi and Yousuf, 2012).

1 -^

ScHizothorax esocinus Meckel, 1838

Kingdom Animalia

Phylum Chordata


Superclass Pisces

Class Osteichthyes



Order Cypriniformes

Family Cyprinidae


Genus Schizothorax

Species esocinus

Schizotliorax esocinus (Heckel, 1838)

Common names

Chirruh snowtrout English

Chirruh Kashmiri

Salient features

S. esocinus differs from all other Kashmir valley Schizothoracinae in lower gill raker

number (8-15) and in the much longer jaws, without enlarged lips or tuberculate pads.

Body is elongate, fusifomi with a long snout, only slightly prognathous upper jaw or

jaws equal. A series of enlarged scales along the anal-fm base. Scales are very small,

96-108 in the lateral line (Kullander et al., 1999)

Colour

Colour pattern is distinctive with silvery colour and numerous dark, small irregular

spots on back and flanks of body. Fins silvery-grey, with similar dark spots, more

numerous at their bases.


India: Indus river and its tributaries in Ladakh and Kashmir valley; and Afghanistan

(Talwar and Jhingran, 1991).

Fishery information

This species attains a maximum standard length of about 20 cm (Talwar and Jhingran,

1991). This species occurs in mountain streams, rivers and lakes (Menon, 1999).

Inhabits sandy and gravel-bottomed rivers (Shrestha, 1990). Herbivore, feeding on

bottom detritus. Mature adults undertake spawning migration to incoming streams

where they breed amidst gravel and sandy beds (Raina and Petr, 1999). Fry always

occur in quiet parts of the streams or in the side branches of the main streams

(FishBase, 2012).

14

MATERIALS AND METHODS

1. Fish sampling and data collection

A total of 173 specimens of S. curvifrons (Total length = 18.2-42.9 cm), 126

specimens of 5. niger (Total length = 18.7-37.3 cm) and 199 specimens of 5. esocinus

(Total length = 12.4-61.1 cm) were collected from the Jhelum river and Dal lake of

the Kashmir valley, India from June 2011 to June 2012. The following parameters

were recorded for each individual:

1.1. Total length (TL): Distance in a straight line between the anterior most part

of the body (snout or premaxilla, whichever is making the anterior most extremity of

the body) to the tip of the tail. In case the lobes of the caudal fin differ in length, the

length of larger lobe was taken.

1.2. Fork length (FL): Distance from the anterior most part of the body to the

anterior limit of the median notch or the bifurcation of the caudal fm.

1.3. Standard length (SL): Distance from the tip of the snout or premaxilla to the

base of the caudal fm (hypural joint), where a groove fonns usually when the tail

bends from side to side.

1.4. Weight (W): Total weight of each fish (including gut and gonads) was taken.

Identification of fishes was done following Day (1878) and Kullander et al. (1999).

Length and weight measurements were recorded to the nearest 0.1 cm and 0.1 gm,

respectively.

2. Age reading techniques

Scales, opercular bones, otoliths, vertebrae and cleithra were examined to compare

their age estimates as per standard protocols (Khan and Khan, 2009; Khan et al..

2011 a)

15

2.1. Collection and preparation of scales

A minimum of 10 scales were removed with forceps from under the anterior part of

the dorsal fin. Scales were cleaned by first removing the extraneous matter and

mucous by washing them in tap water and then rubbing in between the finger tips.

They were then mounted between two glass slides and studied with the help of

compound microscope (Tandon and Johal, 1996).

2.2. Collection and preparation of opercular bones

The opercular bones were removed and dipped in boiling water for few minutes to

remove extraneous tissue. A bristled brush was used to remove tissue that boiling

water did not loosen. Cleaned opercular bones were dried at room temperature and

examined under transmitted fluorescent light with naked eye (Phelps et al., 2007;

Khan and Khan, 2009).

2.3. Collection and preparation of otoliths

Otoliths (sagittae) were removed with a pair of fine forceps, rinsed with distilled

water and stored dry in labeled envelopes. Otoliths were read whole by immersion in

glycerol and examined under microscope using reflected light. Otoliths with unclear

annual rings were ground with sandpaper to make the annuli more distinct for age

reading (Tandon and Johal, 1996; Khan and Khan, 2009).

2.4. Collection and preparation of vertebrae

Vertebrae (4" to 10*) were removed and placed in boiling water for 10-15 min to

clear the attached muscles. A bristled brush was used to remove tissues that boiling

water did not loosen. Vertebrae were examined under dissecting microscope using

reflected light (Phelps et al., 2007; Khan and Khan, 2009)

16

2.5. Collection and preparation of cleithra

Cleithra were removed from fresh specimens and the muscles were separated by

dipping them in boiling water for 5 minutes. The cleaned and dried cleithra were

examined under transmitted fluorescent light with a dissecting microscope (Euchner,

1988).

2.6. Measures of precision

Each structure was examined for age estimation independently by two readers. Age

assessments of all the fish samples were done in random order and without prior

infonnation on fish length, weight or date of collection. Such data was utilized to

calculate the precision of age estimation between the two readers. However,

consensus data (from the two readers for the specific structures) was utilized to

compare the age estimates between structures and also to evaluate the statistical

significance among the mean age estimates from different stmctures. A consensus

between readers was required in cases where structures exhibited disagreement in age

assignments by the readers (Khan and Khan, 2009). In S. ciinifrons and S. niger each

alternative structure (scales, opercular bones, vertebrae and cleithra) was paired with

the otoliths (showing high PA and low APE and CV values) and in case of S. csociniis

each alternative structure was paired with vertebrae (showing high PA and low APE

and CV values) to further interpret precision.

Age readings were tested for bias and precision. Age bias plots were constructed to

identify trends and sources of bias in discrepancies between age estimates among

successive readings. Age estimates were compared by calculating the average percent

error (APE), coefficient of variation (CV) and percent agreement (PA) between the

readers and between the pairs of ageing structures (Campana et al., 1995). APE was

derived using the formula presented by Beamish and Foumier (1981):

R I I

APEj = 100% X - ) ' ' " i = l J

Where x,;y is the rth age determination of theyth fish, Xj is the mean estimate of theyth

fish, and R is the number of times each fish is aged. The resulting value represents the

APEj oftheyYhfish.

17

CV, expressed as the ratio of standard deviation over mean, was computed following

Chang (1982):

ivR ^^'i ^y \U=1 R _ l

CVj = 100%x

Where CVj is the age precision estimate for thejth fish. Low values for CV and APE

indicate high levels of precision.

PA between structures was also calculated to further interpret precision and was

estimated as the proportion of each age on which both readers agreed.

3. Growth analysis

3.1. Estimation of growth parameters

To evaluate variability in growth, observed length-at-age data based on otoliths in S.

cun'ifrons and S. niger and vertebrae in S. esocimis were fitted to the von Bertalanffy

gi-owth function (Ricker, 1975), by non-linear least squares regression. The VBGF is

represented as:

Lt = Loo(l-e-k[t~to])

Where L == total length (cm) offish at age t;

Loo = asymptotic mean length;

K = rate constant that deteiTnines the rate at which Lt approaches 1^;

t = time or age of the fish and

tn = the hypothetical age at which the fish had zero length.

VBGF equation was also computed using one of the most common and non-lethal

ageing structure, the scales, in order to compare the VBGF parameters to that

obtained using the precise ageing structure.

The concept of growth performance index introduced by Pauly and Munro (1984)

makes it possible to directly compare the growth performance of different populations

of the same species, based on von Bertalanffy growth parameters. The performance

Index (0) is calculated as:

18

0 = logioK + 21ogioLoo

The performance index was estimated using the growth parameters Loo and K

obtained in this study.

3.2. Length-weight relationship

Length-weight relationships were determined by logarithmic transformation of the

linear regression equation:

log W = log a + b log SL

Where:

W = weight of the fish (g);

SL = standard length (cm);

a = intercept and

b = slope of the regression curve or growth coefficient

The degree of association between the variables was computed by the detemiination

coefficient, r". Additionally, 95% confidence limits (CL) of a and b were estimated.

3.3. Length-length relationship

Length-length relationships viz. total length vs standard length, standard length vs

fork length and fork length vs total length were calculated by linear regressions

(Hossain, 2010).

3.4. Condition factor

Condition factor is a quantitative parameter of the state of well-being of the fish that

will detennine present and future population success by its influence on growth,

reproduction and survival. The Fulton's condition factor (K) was calculated according

to the equation:

K=(W/SL^)x 100

Where:

W = weight of fish in grams

SL = standard length of fish in centimeters

A plump fish will show a larger ratio than a thin or lean fish of same length.

19

4. Data analysis

For each fish species, the data obtained on age estimation from different hard

anatomical parts were subjected to Pearson's correlation analysis between the

structures in order to establish the relationship among readings of different structures

of the same fish species. Percent agreement was calculated using the "Templates for

calculating ageing precision" by Sutherland (2006). Mean age readings (consensus

data) obtained from various bony structures were subjected to one-way analysis of

variance (ANOVA) followed by Duncan's multiple range test (DMRT) (Gomez and

Gomez, 1984) in order to explain whether the readings from different bony structures

of the same species showed significant differences among themselves (Khan and

Khan, 2009). Growth Parameters were estimated using non-linear regression methods,

as implemented in a Microsoft Excel based application developed by Cope and Punt

(2007). Length-weight and length-length relationship of the fish was examined by

simple linear regression analysis.

All statistical analyses were done using MS-Excel and SPSS (version 12.0).

20

Results

1. Age estimation

The precision of age estimates from different readers as well as different structures

showed variations within and among species. In Schizopyge curvifrons and

Schizopyge niger, highest mean age values were obtained from otoliths and lowest

from cleithra while in Schizothorax esocinus, vertebrae exhibited highest values of

mean age estimates while cleithra exhibited the lowest values. The relative precision

of age detemiination between readers and between structures were estimated using the

percent agreement (PA), the average percent error (APE) and the average coefficient

of variation (CV) as presented in Table 1 and 2.

1.1. Schizopyge curvifrons

In S. curvifrons, the specimens ranged in age from 1 to 6 years. Percent agreement

(PA) between the two independent readers was highest for the otoliths (95.4%)

followed by opercular bones (93.6%), vertebrae (91.3%), scales (86.1%) and cleithra

(82.7%) (Table 1). Between structures, highest PA was found between otoliths aiul

opercular bones (88.4%), followed by vertebrae (82.1%), scales (74.0%) and cleithra

(68.8%) (Table 2). In S. curvifrons, otoliths and opercular bones showed lov\est

values of APE and CV as compared to other structures substantiating high precision

in detecting annuli. There was no ageing bias between readers for otoliths while little

ageing bias was found between age estimates from scales and cleithra as shown by the

age bias graph (Fig. 1). Age bias graphs between structures revealed no age bias when

otoliths were compared to opercular bones and vertebrae whereas underestimation of

age was found with scales and cleithra for older fish species (Fig. 4).

The correlation coefficient between readers was higher for otoliths (0.977) and

opercular bones (0.970) as compared to other structures (Table 3). Similarly,

correlation coefficient between age estimates from different bony parts of S.

curvifrons showed that each ageing structure was correlated significantly (P<0.01)

with the other. Correlation coefficient between otoliths and opercular bones indicated

a near perfect concordance of age estimates from the two structures (0.937). Mean

values of age estimates from different structures, when compared using ANOVA

21

followed by DMRT, showed highest (P < 0.01) values for age readings from otoliths

followed by opercular bones, vertebrae, scales and cleithra (Table 4). Age readings

from otoliths, opercular bones and vertebrae did not show any significant (P < 0.01)

differences.

1.2. Schizopyge niger

In S. niger, PA of ages between readers was higher for otoliths (94.6%) than scales

(92.3%), vertebrae (84.6%), opercular bones (82.3%) and cleithra (80.0%) (Table 1).

When otoliths age estimates were compared with other structures, highest PA was

found between otoliths and scales (86.9%) followed by vertebrae (83.8%), opercular

bones (78.5%) and cleithra (73.8%) (Table 2). Otoliths and scales showed lowest

values of APE and CV as compared to other structures. No age bias was present

between readers for otoliths, scales and vertebrae while little ageing bias was found in

opercular bones and cleithra (Fig. 2). Between structures, little age bias was present

when otoliths were compared to scales, vertebrae and opercular bones whereas

cleithra showed underestimation of age (Fig. 5).

Correlation coefficient between readers was higher for otoliths (0.978) and

scales (0.970) as compared to other structures (Table 3). Correlation coefficient

between age estimates from different bony parts of S. niger showed that each part was

significantly (P < 0.01) correlated with the other. Otoliths exhibited highest values of

correlation with the scales (0.946) followed by vertebrae (0.924), opercular bones

(0.913) and cleithra (0.896). Mean values of age estimates from different structures

shovv'ed that age estimates obtained from otoliths were significantly (P < 0.05) higher

than that from cleithra but comparable (P < 0.05) to the values from scales, vertebrae

and opercular bones (Table 4).

1.3. Schizothorax esocinus

Between readers agreement for vertebrae was higher (96.0%) than opercular bones

(95.0%), scales (93.5%), otoliths (90.5%) and cleithra (87.4%) (Table 1). When age

estimates from vertebrae were compared with other structures, highest PA was found

between vertebrae and opercular bones (87.9%) followed by scales (86.4%)), otoliths

22

(80.9%) and cleithra (73.9%) (Table 2). Vertebrae, opercular bones and scales showed

low values of APE and CV. No indication of reader bias was noted for any structure

(Fig. 3). Between structures, little bias in age estimation was noted between vertebrae

and cleithra (Fig. 6) with cleithra showing underestimation of age in older fish.

The correlation coefficient between readers was also higher for vertebrae

(0.994) as compared to other structures (Table 3). In S. esocinus, correlation

coefficient between age estimates from different bony structures showed that each

part was correlated significantly (P < 0.01) with the other; highest values were found

between vertebrae and scales (0.974) followed by opercular bones (0.972), otoliths

(0.960) and cleithra (0.945). Mean values of age estimates from different structures

showed that values obtained from cleithra were significantly (P < 0.05) lower than the

readings obtained from all other structures except otoliths (Table 4). Also, the age

readings from vertebrae, opercular bones, scales and otoliths were comparable

(P<0.05) with each other.

2. Growth

2.1. Growth parameters

The von Bertalanffy growth parameters as well as growth perfonnance index (0) m

the selected fish species are presented in Table 5.

S. curx'ifrons

Following growth equation emerged using otoliths as the ageing structure:

Lt = 49.8 (1 - e-o-263(t+o.34>)

iS*. niger

Von Bertalanffy growth curve was fitted to the total length at age data using otoliths.

Following growth equafion was obtained:

Lt = 44.8 (1 - e-0-255(t+i.42)^

S. esocinus

The VBGF parameters obtained using vertebrae have been presented in the following

equation:

23

Lt = 66.6 (1 - e-o-27^ (t+o.34))

The von Bertalanffy growth curve is shown in Figure 7. Greater predicted

lengths for older specimens were estimated from scale-aged than otolith-aged fish.

The von Bertalanffy growth parameters constructed with scale data had a higher

asymptotic length and a lower growth coefficient than those found in the model based

on otoliths in S. curvifrons and S. niger and vertebrae in 5*. esocinus. Growth

performance index was found to be highest for S. esocinus (3.09) followed by S.

curvifrons (2.81) and S. niger (2.71), respectively.

2.2. Length-weight relationship

Length-weight data are presented in Table 6. The length-weight relationships were

calculated and represented in the form of following equations:

S. curvifrons Log W = -1.401 -|- 2.69 Log SL (n = 136: r = 0.992)

S. niger Log W = -1.304 + 2.66 Log SL (n = 173: r '= 0.982)

S. esocinus Log W = -1.925 + 3.08 Log SL (n = 163: r^- 0.995)

2.3. Length-length relationship

Estimated parameters of the LLRs are given in Table 7. The LLRs were calculated

and represented in the form of following equations:

.S". curvifrons TL = 2.39 -f- 1.09SL r = 0.998

FL = 1.68 + 1.04SL r = 0.999

TL = 0.63 + 1.05FL r^= 0.999

S. niger TL = 2.23 + l . l lSL ? = 0.993

FL= 1.38 + 1.06SL r^= 0.997

TL = 0.75-I-1.05FL r^= 0.997

S. esocinus TL = 0.93 + 1.15SL r^= 0.998

FL = 0.45-t-1.08SL r^= 0.997

24

TL = 0.48 + 1.06FL r^= 0.998

2.4. Condition factor

Condition factor (K) was found to be highest for S. niger (mean 0.49) and lowest for

S. curvifrons (mean 0.49).

S. curvifrons K = 0.49 (0.18-1.20)

S. niger K = 1.74 (1.24-2.01)

S.esociniis K = 1.51 (1.24-1.85)

25

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DISCUSSION

When assessing methods for age determination in fishes, it is important to consider

both accuracy and precision. Imprecise age estimates suggest variabiHty in ageing

criteria or the presence of unclear annuH that are difficuh to distinguish and count,

while inaccurate age estimates bias population parameters such as growth and

mortality (Quinn and Deriso, 1999). Despite the call for more statistically robust and

consistent analysis of ageing data in recent years (Beamish and Foumier, 1981;

Chang, 1982; Campana et al., 1994; Jackson et a!., 2007), many studies report

population data (i.e. length-at-age) without mention of the precision of their age

estimates. In the first study on precision of age estimates in S. cnrvifrons, S. niger and

S. esocinus inhabiting Kashmir valley, it v/as observed that the structures giving

precise age estimates varied among the selected fish species.

Otoliths

Agreement between age estimates from otoliths and other hard structures varied

among species as well as between readers (Table 1 and Table 2). In general, we found

that otoliths yielded the most precise age estimates for S. cunnfrons and S. niger with

age agreement between readers to be 95.4% and 94.6%. Studies have consistently

shown higher precision in ages assigned with otoliths than with scales. This is in

accordance to a mounting body of evidence that the scale method of age estimation

for fishes belonging to subfamily Schizothoracinae may be unreliable (Zhao et al..

1975; Li et al., 2009; Chen et al., 2009; Ma et al, 2011). Otoliths were reported to

provide the most reliable age estimation, while the annuli on vertebrae and opercular

bones were not very clear in Gymnocypris selineuoensis (Chen et al., 2002a, b; Ma et

al., 2011). Otoliths continue to grow and form annuli even as body growth slows and

asymptotic length is reached, and annuli reabsorption does not appear to occur during

periods of food limitation or stress (DeVries and Frie, 1996; Maceina and Sammons,

2006). Otoliths were reported to be the best structure for estimating yellow perch age

based on high reader agreement and low coefficient of variafion (CV) (Niewinski and

Ferreri, 1999). Gumus et al. (2007) determined age and growth of Scardinius

erythrophthalmus (Linnaeus, 1758) using five hard structures (scales, vertebrae,

opercular bones, lagenar and utricular otoliths) and reported otoliths as most reliable

26 . . . . . . ,

ageing structure. Isermann et al. (2003) demonstrated that whole-view otoliths were a

more time efficient method for ageing walleyes than scales or dorsal spines.

Boxrucker (1986) and Kruse et al. (1993) also suggested that ageing whole-view

otoliths was less time-consuming. Ages estimated from scales and spines were less

precise than from otoliths and scale ages showed underestimation in older specimens

of largemouth bass, smallmouth bass, yellow perch and brown bullheads collected

from upper Hudson river located in north-eastern USA (Maceina and Sammons,

2006).

Vertebrae

Amongst all age structures, vertebrae were found to be the most suitable ageing

structure in S. esocinus, with agreement of age estimates between readers to be

96.0%. The findings were similar to those of Ma et al. (2011) who reported that age

estimates of S. o 'connori from vertebrae and otoliths matched closely while opercular

bones appeared to underestimate age but for older fish, the counts diverged and

otoliths consistently provided higher age estimates. Filmalter et al. (2009) compared

otoliths and vertebrae as potential hard structures for ageing South African yellow fin

tuna, Thunnus albacares and found that growth increment counts from whole otoliths,

sectioned otoliths and vertebrae were not significantly different (t-test, p > 0.05).

Khan et al. (2011b) compared age estimates from otoliths, vertebrae, and pectoral

spines in African sharptooth catfish, Clarias gariepinus (Burchell) and found that

mean age estimates from otoliths were comparable (P > 0.05) to the values obtained

from vertebrae. Guinn and Hallberg (1990) reported that vertebrae and otoliths gave

similar age esfimates in Burbot, Lota lota (Linnaeus). Vertebrae were the most

reliable bony structure for ageing shad {Alosa pontica Eichwald, 1838) inhabiting the

Black Sea, as it had the highest agreement and the lowest ageing error (Yilmaz and

Polat, 2002). The findings of Liu et al. (2009) indicate that the vertebrae are suitable

calcified structure for age determination of the sharptail mola.

Scales

In S. niger, when otoliths age estimates were compared with other ageing structures

(i.e., scales, opercular bones, vertebrae and cleithra), highest PA (86.9%) and lowest

27

APE (3.61%) and CV (5.10%) values were reported between otoliths and scales. In

most of the cyprinids, age has been estimated from scales (Kamilov, 1984; Phelps et

al., 2007). In addition to having clear and sharp annuli, scales also have the

advantages such as easy collection, preparation and being non-destructive to the fish

(DeVries and Frie, 1996). Because scales are commonly used to age fish, numerous

studies have assessed the accuracy and precision of scale age (e.g., Erickson, 1983;

Boxrucker, 1986; Kruse et al., 1993; Long and Fisher, 2001). Amongst all age

structures, scales were found to be the most suitable ageing structure in L. rohita and

C. marulius (Khan and Khan, 2009). Precision of ages detennined from scales and

otoliths were similar in black crappies collected from South Dakota waters (Kruse et

al., 1993). Several researchers have reported that scales can provide unreliable

estimates of fish age (Boxrucker, 1986; Hammers and Miranda, 1991; Khan and

Khan, 2009). Scale ages were on an average 9 years less than the ages estimated from

sectioned otoliths in Morone saxatilis (Linnaeus) older than 20 years, but scales were

reported to esfimate age adequately up to the age of 12 years (Secor et al., 1995). In

some scienfific reports, the use of scales had been criticized mainly because of the

frequent underesfimation of the ages in older fish (Beamish and McFarlane, 1987).

Imprecise age enumeration from scales has been attributed to reabsorption and

deposition of false annuli due to stress and food limitation, and annuli becoming

obscure because scale growth tends to cease as fish grow older (Beamish and

McFarlane, 1987; DeVries and Frie, 1996; Maceina and Sammons, 2006).

Opercular bones

Esfimates from otoliths in S. curvifrons were compared with other ageing structures

(i.e., scales, opercular bones, vertebrae and cleithra) and were found to match closely

with opercular bones with highest PA (88.4%) and lowest APE (1.75%) and CV

(2.47%) values. Age bias graphs between structures (Figure 4) indicated that age

estimates obtained from otoliths and opercular bones were in a good agreement. Khan

and Khan (2009) suggested that annuli in opercular bones provided the precise age

estimation in Catla catla. Opercular bones were reported to be superior to scales for

the age estimafion of common carp (McConnell, 1952). The determination of age and

growth of fish from opercular bones is well established in a number of fishes and have

more reliable age estimates than scales, vertebrae, spines or other hard parts in Esox

28

lucius (Linnaeus) (Frost and Kipling, 1959). In S. niger and S. esocinus annuli on

opercular bones showed mean age estimates comparable to those from all other

structures except cleithra while in S. curvifrons mean age estimates from opercular

bones were comparable to all other structures except scales and cleithra.

Cleithra

Cleithra are commonly used to age fishes (e.g., Casselman and Crossman, 1986;

Sharp and Bernard, 1988; DeVries and Frie, 1996; Quist et. al., 2007); however, few

studies have been conducted to evaluate the precision among age estimates using

cleithra. Govind and Gopal (1966) found valid growth rings in the cleithral bone of

Silonia childrenii. Laine et al. (1991) noted that scales are not as well-suited for use in

age determination of pike as compared to cleithra. Brennan and Cailliet (1989)

evaluated a variety of calcified age structures (pectoral fin rays, opercles, clavicles,

cleithra, medial nuchals, and dorsal scutes) used to age white sturgeon Acipenser

transmontanus and found that ages estimated from these structures did not vary

significantly. However, in the present study, mean values of age estimates from

cleithra was found to be significantly different to those from all other structures

except scales in S. curvifrons, opercular bones in S. niger and otoliths in S esocinus.

Nuevo et al. (2004) found otoliths and cleithra to be unsuitable structures for age

deteraiination of bighead carp from the Mississippi River. Quist et al. (2007)

evaluated between reader precision and agreement of otoliths age estimates from

scales, fin rays, cleithra, and opercular bones and found that exact agreement between

readers was highest for otoliths and fin rays and lowest for opercular bones, cleithra,

and scales.

Growth parameters

Estimates of the size of fish in relation to age (time) are used for estimating certain

growth parameters. Each of these parameters describes the inherent characteristics of

growth of the species. The von Bertalanffy growth function is commonly used in

describing fish growth (Gallucci and Quinn, 1979; Misra, 1980; Chen et al, 1992).

This function has only three parameters, making it statistically robust compared to

models with more parameters (Booth, 1997). The VBGF parameters are commonly

29

used in mortality estimates and fisheries stock assessment modelling (Dominguez et

al., 2006). The von Bertalanffy equation follows the assumption that fish grows

towards some theoretical maximum length, and the growth rate declines as the fish

reaches its ultimate length (Beverton and Holt, 1957).

The growth coefficient (k) is a useful index for estimating the potential

vulnerability of stocks to excessive exploitation and for comparing life history

strategies (Pratt and Casey, 1990; Musick, 1999). Branstetter (1987) categorized the k

values as 0.05-0.10/year for slow growth species, 0.10-0.20/year for species with

moderate growth, and 0.20-0.50/year for rapid growth. In the present study, the value

of K was in the range of 0.20-0.30/year. A high value of k indicates a high metabolic

rate and such fishes mature at an early age or at a size which is large in relation to

their asymptotic length, LQO (Qasim, 1973).

The Loo of S. niger (44.8 cm) was larger than the maximum obser\'ed size of

37.3 cm which was likely due to the less number of large specimens. Growth model

estimates are greatly affected by the lack of very young or old individuals (Cailliet

and Goldman, 2004; Ma et al., 2010). In S. ciirvifrons (N=-173) and S. esociniis

(N=199) due to relatively high sample size and rather good agreement of Lx with the

observed maximum length, values appear to be more reliable and clearly underline the

trend of higher growth coefficients in smaller sized species. This in coiToboration

with the findings of Frisk et al. (2001).

In general, growth parameters need to be checked for quality and validity

(Karlou-Riga and Sinis, 1997), while a negative value close to zero for to is a good

indicator of the reliability of the determined ages (Kerstan, 1985; Gang et al., 2008).

The estimate of to in the present study ranged from -0.30 to -1.45, minimum for 5.

esocimis (-1.42) and maximum for 5'. curvifrons (-0.34).

Growth performance values were all in the same range, as should be expected

for related species, but still there was variation between species. In S. esocinus, which

also had the highest k value, growth performance was found to be highest (3.09)

fohowed by S. curvifrons (2.81) and S. niger (2.71).

The growth parameters may vary regionally or methodologically; it also

depends on differences in size of the largest individual sampled, species, sex and age.

VBGF parameters were generated using otoliths and scales in both S. curxnfrons (PA

30

74.0%) and S. niger (PA 86.9%) in order to compare the results from the two studies.

Scales were selected because they are often the most common structure for age

estimation on account of their advantages discussed elsewhere. The length-at-age data

derived from otoliths and scales were significantly different in S. curvifrons (t-test for

paired comparison; t = 3.159, df = 5, p < 0.05) but no significant difference was found

in S. niger (t = 2.588, df = 4, p > 0.05). In S. esocinus, VBGF parameters were

generated using vertebrae and scales (PA 86.4%) in order to compare the results from

the two studies. The mean total length derived from vertebrae and scales were

compared but no significant difference was found (t-test for paired comparison; t =

2.562, df = 5, p > 0.05). Estimates of asyinptotic length derived from scales were

higher for both species together with a moderate growth coefficient that shows that

their size increased at similar ages. However, the method of age detennination from

scales could be still applicable to analysis of growth for these species, because of

similar growth performance indices. These results suggest that management actions

based on estimates of growth would not be significantly influenced by the type of

structure used.

Length-weight relationship (LWR) and length-length relationship (LLR)

No infonnation on LWRs and LLRs of the selected fish species was available in

FishBase (Froese and Pauly, 2011). When the b value in LWR was equal to or did not

show statistically significant deviation from 3, the growth was isometric, whereas the

positive or negative allometric growth occurred when the b value deviated

significantly from 3: positive if b > 3 and negative if b < 3 (Ricker, 1975). The LWRs

suggested isometric growth in S. esocinus (3.08) which was in agreement to the

reports of Bhagat and Sunder, 1984 (3.0034), Bhat et al., 2010 (3.0034) and Dar et al.,

2012 (2.7148 for males and 2.8618 for females) respectively. The negative allometric

growth for the remaining species implies that the allocation of energy is more towards

axial growth rather than to biomass. In S. curvifrons, the allometric coefficient b of

the LWR was reported to be negatively allometric (b < 3) throughout the year except

March, July and October where the growth was isometric (b=3) (Mir et al., 2012).

Shafi and Yousuf (2012) reported the value of b for S. niger as 3.07 for males, while

in females it was 2.77 and in case of pooled data its value was 3.07. The value of b

reported by Shafi and Yousuf (2012) for S. niger is different from the present study

31

which can possibly be due to several factors such as the habitat, number of specimens

examined and length ranges and length types used. As per the data available in

FishBase (2011), we reported the new maximum standard length for S. esocinus (50.8

cm) and S. niger (32.6 cm). As suggested by Petrakis and Stergiou (1995), use of

LWRs should be strictly limited to the observed length ranges applied in the

estimation of the linear regression parameters. All LLRs were highly significant (P <

0.001), with determination coefficients (r^) > 0.98.

Condition factor (K)

The most useful tools used for evaluation of fish populations, are the mathematical

equations or parameters intended to estimate fish condition, using the relation

between total length and weight (Le Cren, 1951, Bolger and Connolly, 1989,

Ritterbusch-Nauwerck, 1995). The condition factor (K) is an index reflecting

interaction between biotic and abiotic factors in the phvsiological condition of the

fishes. It shows the well-being of the population during various life cycle stages

(Angelescu et al., 1958; Gupta et al., 2011). The condition of 5'. curvifrons and 5.

esocinus from Jhelum river and 5. niger from Dal lake of Kashmir valley was

evaluated using the Fulton"s condition factor. The values obtained tilted the range of

values most commonly reported for these species. In S. curvifrons, the condition

factor was calculated month-wise and it ranged from 1.0-1.95 (Mir et al., 2012). Shafi

and Yousuf (2012) reported Fulton's condition factor for S. niger in the range 0.996-

12.4 (minimum of 0.996 in November and maximum of 1.24 in March). Sex-wise

analysis of 'K„' values in S. esocinus revealed that the mean 'K,,' value was 0.96 in

females and 0.91 in males (Dar et al., 2012). Slight differences in the mean values

between the results obtained and the published data could be the result of different

seasons at capture and the fact that the influence of fish length on the condifion factor

was not taken into consideration in the analyses. According to Le Cren (1951), 'K,,'

greater than 1 indicated good general condition of fish. Pandey & Sharma (1997)

studied the condition of four exofic carps and only the common carp, Cyprinus carpio

communis was found to have value above 1 ( 1.0109). Pandey & Sharma, 1998

reported high 'K ' values for Labeo rohita (1.0129) and C. catla (1.0007) and low

values for Cirrhinus mrigala (0.9967).

32

It may be concluded from the present study that otoUths were the most precise

ageing structure in S. curvifrons and S. niger while vertebrae showed most clear and

sharp rings in S. esocinus. The estimated ages were 1-6 years for S. curvifrons and S.

esocinus and 1-5 years for S. niger. The von Bertalanffy growth model was obtained

as Lt = 49.8 ( l - e-0'263(t+o.34^ -j ^ curvifrons, Lt = 44.8 (1 - e-o-255(t+i.42)^ i^ ^

niger and Lt = 66.6 (1 - e"°-^^^ (t+0.34) -^^ esocinus. The von Bertalanffy growth

parameters were significantly different between otoliths and scales in S. curvifrons but

did not differ significantly between otoliths and scales in S. niger and between

vertebrae and scales in 5. esocinus. The study of LWR in selected fish species showed

an almost isometric pattern of growth in S. esocinus while in S. curvifrons and S.

niger the value of b was found to be negatively allometric. Estimated parameters of

the LLRs were highly significant (P < 0.001), with detemiination coefficients (r^) >

0.98. K in the selected fish showed values within the range 0.18-1.20 in S. curvifrons,

1.24-2.01 in S. niger and 1.24-1.85 in S. esocinus.

33

Q^ummaty

SUMMARY

The present study was undertaken with a view to evaluate and compare age estimates

from different ageing structures (scales, opercular bones, otoliths, vertebrae and

cleithra); to fit the length-at-age data to the von Bertalanffy growth model; and to

investigate the length-weight, length-length relationships and condition factor in

Schizopyge curvifrons, Schizopyge niger and Shizothorax esocinus. Standard

procedures were followed to prepare and study the ageing structures. The age and

total length data were used for estimating the parameters of von Bertalanffy growth

equation. Body measurements were taken as per the standard procedures to study

length-weight, length-length relationships and condition factor. In S. curvifrons and S.

niger, percent agreement between-readers was highest for otoliths i.e. 95.4% and

94.6%, respectively and in S. esocinus, percent agreement was highest for vertebrae

(96.0%). When otolith ages were compared with other alternative structures viz.,

scales, opercular bones, vertebrae and cleithra highest percent agreement was found

between otoliths and opercular bones (88.4%) in S. cur\nfrons and between otoliths

and scales (86.9%) in S. niger. In S. esocinus, highest agi'eement was found between

vertebrae and opercular bones (87.9%). Otoliths exhibited highest values (P < 0.05) of

mean age estimates in S. cunifrons and S. niger while in S. esocinus highest \alues of

mean age estimates were found for vertebrae. Correlation coefficient of age

estimation from different bony parts of S. cur\nfrons, S. niger and S. esocinus showed

that age estimates from all the age structures were significantly (P < 0.01) coixelated

with each other. The von Bertalanffy model growth parameters were estimated as L^

- 49.8, K = 0.263, to = -0.34 for S. curvifrons; Loo= 44.8, K = 0.255, to = -1.42 for S.

niger and Loo = 66.6, K = 0.278, to = -0.34 for S. esocinus. The length-weight

relationship equations were: Log W = -1.40 -I- 2.69 Log SL (S. curvifrons); Log W =

-1.30 -I- 2.66 LogSL (S. niger) and Log W = -1.92 -I- 3.08 Log SL (5. esocinus).

Results for length-length relationships for selected fish species indicated that the

values between total length and standard length; fork length and total length, and;

standard length and fork length were highly correlated (r > 0.9). The mean condition

factor of S. curvifrons, S. niger and S. esocinus was 0.49, 1.74 and 1.51, respectively.

34

C^^ermces

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J. Appl. Ichthyol. 29 (2013), 283-284 © 2012 Blackwell Veriag GmbH ISSN0175-S659

Received: February 5, 2012 Accepted: April 4, 2012

doi: 10.1111/j.1439-0426.2012.02061 ,x

Technical contribution

Length-weight and length-length relationships for five fish species from Kashmir VaUey By Mohammad Afzal Khan and Sabah

Department of Zoology. Section of Fishery Science and Aquaculture, Aligarh Muslim University, Aligarh, India

Summary Length-weight (LWR) and length-length relationships (LLR) are presented for two species of Schizopyge [S. curvi-frons (Meckel, 1838) and S. niger (Heckel, 1838)] and three species of Schizothorax [S. esocinus (Heckel, 1838), S. labiatus (McCleUand, 1842) and S. plagiostomus (Heckel, 1838)] from the Kashmir valley o( India. A total of TiS specimens were sampled and measured from June to December 2011. No information regarding LWRs and LLRs of these species was available in FishBase.

IntrodnctioD

Knowledge on length-weight (LWR) and length-length relationships (LLR) is useful in fish slock and popxUation assessments (Ricker, 1968; Kara and Bayhan, 2008). Size conversions (e.g. calculated TL from Sh) are needed for comparison of species. The present study was undertaken with the objective to estimate the length-weight and length-length relationships for five fish species collected from the Jhelum River and Dal Lake of the Kashmir valley in India.

Materials and mediods

Data on length and weight of S. curvifrons, S. esocinus, S. labiatm, and S. plagiostomus from the Jhelum River and S. niger from Dal lake (Kashmir valley, India) were collected from June to December 2011. Total length (TL), standard

length (SL) and fork length (FL) to the nearest O.i cm and weight (W) to the nearest 0.1 g were recorded for each individual. Identification of fishes was done foffowing Day (1878) and Knllander et al. (1999).

Length-weights were determined by logarithmic transformation of the Unear regression equation; log W = log a + b log SL, where W is the weight of the fish (g), SL is the standard length (cm), a is the intercept and b the slope of the regression curve (Ruiz-Campos et al., 2010). The degree of association between the variables was computed by the determination coeffcient, r^ (Golzarianpour et al., 2011). LLRs viz. TL vs SL, SL vs FL and FL vs TL were calculated by linear regressions (Hossain, 2010). All statistical analyses were done using SPSS version 16.0 (IBM Corporation, Chicago, IL).

Results and discussion

Length-weight statistics for two species of Schizopyge and three species of Schizothorax are presented in Table I. The negative allometric growth for three species imphes that the allocation of energy is more toward axial growth rather than to isometric growth. This may be due to a number of biological factors that are known to influence LWR (Gonzalez-Acosta et a/., 2004; Ruiz-Campos et a/., 2006); however, these factors were not accounted for in the present study. Estimated parameters of the LLRs are given in Table 2. As expected, the TL was roughly 10% longer than SL.

Table 1 Estimated parameters of LWR for two species of Schizopyge and three species of Schizothorax: in bold, new maximum length records not found to date in electronic data bank FisbBase.oig

Length (cm)

range

Length Scientific name Study N Min Max a 95% CL b 95% CL ,2 type

Schizopyge Present study 136 14.5 37.0 0.039* 0.028-0.056 2.69 2.582-2.798 0.992 SL curvifrons

Schizopyge niger Present study 173 14.7 32.6 0.049* 0.026-0.093 2.66 2.453-2.864 0.982 SL Schizothorax Present study 163 10.3 50.8 O.OU* 0.008-0.016 3.08 2.98-3.17 0.995 SL esocinus Bhagat and Sunder,

1984; 187 U.O 55.6 -~5.10 — 3.02 - 0.956 TL

Bhat et al., 2010 70 5.7 42.0 -^5.16 - 3.00 - - TL Schizothorax Present study 142 17.6 38.7 0.044* 0.019-0.993 2.64 2.39-2.89 0.972 SL

labiatus Bhatet al., 2010; 40 9.2 25.5 -5.25 - 3.09 - - TL Schizothorax Present study 121 18.5 41.5 0.022' 0.011-0.042 2.86 2.66-3.05 0.982 SL plagiostomus Bhatet al., 2010 136 9.6 52.0 -4.96 - 2.95 - - TL

N, total number of samples; a, intercept; b, slope; CL, Coafsdeace hmits; r^. Coefficient of determination. *Anti-log a.

IJ.S. Copyright Qearance Cealre Code Statement. 0 n 5 - 8 6 5 9 / 2 O l 3 / 2 9 O l - 2 8 3 $ 1 5 . 0 0 / 0

284 M. Afzal Khan and Sabah

Table 2 LLRs between total length (TL), fork length (FL) and standard length (SL) for two species of Schizopyge andthree species of Schizo-thorax

Species N Equation a b r"

Schizopyge 136 TL=a + bSL 2.39 1.09 0.998 cunrifrons FL=a + bSL 1.68 1.04 0.999

TL=a + bPL 0.63 1.05 0.999 Schizopyge 173 TL=a + bSL 2.23 1.11 0.993

niger FL=a + bSL 1.38 1.06 0.997 TL=a + bFL 0.75 1.05 0.997

Schizothorax 163 TL=a + bSL 0.93 1.15 0.998 esocinus FL=a + bSL 0.45 1.08 0.997

TL=a + bFL 0.48 1.06 0.998 Schizothorax 142 TL=a + bSL 1.53 1.11 0.998

labiatus FL=a + bSL 0.82 1.061 0.996 TL=a + bFL 0.80 1.05 0.997

Schizothorax 121 TL=a + bSL 2.20 1.08 0.996 plagiostomus FL=a + bSL 0.64 1.06 0.998

TL=a + bFL 1.53 1.02 0.999

N, total number of samples; TL, total length; FL, fork length; SL, standard length; r^, coefficient of determination.

No information on LWRs and LLRs of the selected fish species was available in FishBase (Froese and Pauly, 2011). However, Bhat et al. (2010) reported values of b for S. esocinus (3.0034), S. labiatus (3.0997) and S. plagiostomus (2.9467) in the Lidder River of Kashmir. Bhagat and Stmder (1984) reported the value of b parameter for S. esocinus as 3.0034. The value of b reported by Bhat et al. (2010) for S. labiatus is different from the present study, which is possibly due to several factors such as the habitat, number of specimens examined and length ranges and length types used. As per the data available in FishBase (2011), reported herein is the new maicimnm standard length for S. esocinus (50.8 cm), S. labiatus (38.7 cm), S. plagiostomus (41.5 cm) and Schizopyge niger (32.6 cm). However, Bhat et al. (2010) reported a higher maximum length (TL = 52 cm) for S. plagiostomus. As suggested by Petrakis and Stergiou (1995), use of LWRs should be strictly limited to the observed length ranges applied in the estimation of the linear regression parameters.

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Author's address: Mohammad Afzal Khan, Section of Fishery Science & Aquaculture, Department of Zoolog>', Ali-garh Muslim University, Aligarh - 202 002, India. E-mail: [email protected]

Acknowledgements

The authors are thankful to the Chainnan, Department of Zoology, Aligarh Muslim University, Aligarh, India for providing the necessary facilities for the study.


mailto:[email protected]

1 Using five calcified structures to describe age and growth of three fish species from

2 Kashmir Valley

4 Sabah and Mohammad Afzal Khan*

5 * Corresponding author.

6 E-mail address: khanmatzal(@yahoo.com. (M. Afzal Khan)

7 Abstract

8 Schizothoracinae are the most important food fish of Kashmir valley. Age determination

9 methods and growth rates are poorly described for these species. The present study estimated

10 the precision of age estimates between different structures (scales, opercular bones, otoliths.

11 vertebrae, cleithra) by calculating the percentage of agreement (PA), average percentage of

12 error (APE), and coefficient of variation (CV). Maximum ages of 6 years were observed for

13 Schizopyge curvifrom and Schizopyge niger and 5 years for Schizolhorax esociniis.

14 respectively. In S. curvifrons and S. niger, percent agreement between-readers was highest for

15 otoliths i.e. 95.4% and 94.6% respectively and in S. esocimis. percent agreement was highest

16 for vertebrae (96.0%). The von Bertalanffy growth parameters were as follows: Loo = 49.8

17 cm, K = 0.263 year"' and to =-0.34 year for S. curvifrons (based upon otoliths). Loo= 44.8 cm.

18 K = 0.255 year"' and to = -1.42 year for S. niger (based upon otoliths), and Loo = 66.6 cm. K =

19 0.278 year" and to = -0.34 year for S. esocinus (based upon vertebrae).

20 Keywords

21 Precision. Growth. Schizopyge curvifrons. Schizopyge niger, Schizolhorax esocinus.

22 Communicated for publication in the journal, Ichthyological research (Springer

23 publication).

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