Assessing the quality and value of Parapercis colias nurseries in the

Marlborough Sounds, New Zealand

Andy Xiaoxian Chang

A thesis
submitted to Victoria University of Wellington
in partial fulfillment of the requirements for the degree of
Master of Science in Marine Biology

School of Biological Sciences

Victoria University of Wellington
2021
ii
 Abstract

Coastal nursery habitats are critical for maintaining the populations of many of New Zealand’s
most important fisheries species. Changes in the availability and quality of nursery habitats in
response to anthropogenic activities may be affecting the number of fish that successfully
recruit into adult populations. It is therefore important to identify which habitats are the most
important nurseries, what qualities make them valuable, and how we can protect and restore
them to support fish stocks. Parapercis colias are an important commercial and recreational
fishery species found mostly around the South Island of New Zealand. Juveniles and adults
spend most of their lives on the seafloor, where they depend on biogenic habitats for food
and shelter. The Marlborough Sounds has been a popular fishing ground for P. colias since
the 1900s, but has also been exposed to destructive fishing activities such as commercial
shellfish dredging, which have caused damage to biogenic habitats. Although previous studies
have observed interactions between adult P. colias and their habitats, juvenile habitat
associations have been rarely explored. Additionally, no studies have explored the qualities
of valuable P. colias nurseries. In this thesis, I quantified the growth and diet of juvenile P.
colias collected from a set of nursery habitats in the Marlborough Sounds, New Zealand,
including bryozoan fields, dog cockle beds, horse mussel beds, biogenic clumps, and reef
edges. I used juvenile lengths, weights, and ages to investigate differences in growth among
habitats. I also used juvenile stomach contents to investigate differences in diet among
habitats, specifically focusing on the diversity, abundance, and biomass of prey taxa found.
My results show that not all nursery habitats are equal in value. In particular, reef edges
appear to support significantly faster juvenile growth than other habitats. Juveniles diets
differed in the diversity, abundance, and biomass of prey taxa among habitats. In particular,
juveniles from reef edges consumed more prey items compared to juveniles from other
habitats. Diets were primarily dominated by crustaceans in all habitats, with gammarids and
mysids being particularly important prey items in both abundance and biomass. Knowledge
of the qualities of valuable nursery habitats is critical to the conservation of biogenic habitats
and the management of coastal fisheries. My data will provide important information for the
modelling and management of P. colias stocks in New Zealand, and will help to further our
understanding of how they might respond to changes in the marine environment.

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 Acknowledgements

Firstly, I would like to thank my supervisors Alice Rogers, Jeff Shima, and Mark Morrison for
their continuous advice and support throughout my research. Their encouragement,
patience, and feedback has been instrumental, and I could not have completed this work
without them. Alice, thanks for always dedicating the time to help me, especially when times
were tough, I sincerely appreciate your guidance. Thank you to all the members of the
National Institute of Water and Atmospheric Research (NIWA) sampling team who have
committed tremendous amounts of time collecting and providing the samples used in my
research. It has been an absolute privilege to be a part of Mark’s ‘Juvenile fish habitat
bottlenecks’ research programme, and the amount of passion and work put in by everyone
involved is extremely commendable.

I would like to thank all the members in the Marine Ecology and Ecosystem Modelling (MEEM)
lab for their help and motivation along the way. Tory, Chelsey, Baylee, and Callum, it has been
an extreme pleasure working with you all. Callum, thanks for all the good chats about when
the vis will be good again.

Thank you to everyone at the Wellington University Coastal Ecology Lab (WUCEL), especially
the lab technicians Snout and John. McKenzie, Alice, Valerio, Francesca, Andrea, Ben, Imke
and Alison, thank you all for your support and kindness throughout my time at the lab, I am
privileged to have worked alongside so many talented and hard-working people. Alice, thanks
for showing me the craftsmanship of cold hot chocolates during lunch breaks.

To Alex, Matt, Rose, and everyone else at the university who have shared this rollercoaster of
a journey with me. Thank you for your kind words, love and support, the coffee dates, and
always being up for a lunch break (mostly Matt).

Finally, to my Mum, Dad, and brother Billy, who have been there for me since the beginning
of this journey. Thank you for your continuous love and support, and for driving my passion
in marine life.

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 Table of Contents

Abstract iii
Acknowledgements iv
Table of Contents v
List of Figures vii
1. Introduction 9
1.1. Population dynamics and population bottlenecks in fishes 9
1.2. Pre-settlement sources of mortality 9
1.3. Post-settlement sources of mortality 10
1.4. Juvenile habitats and the role of nurseries 10
1.5. Anthropogenic impacts on nurseries 11
1.6. Parapercis colias in the Marlborough Sounds, New Zealand 12
1.7. Parapercis colias nurseries in the Marlborough Sounds, New Zealand 13
1.7.1. Bryozoan fields 13
1.7.2. Dog cockle beds 14
1.7.3. Horse mussel beds 16
1.7.4. Biogenic clumps 17
1.7.5. Reef edges 18
1.8. Thesis aims 20
2. Differences in juvenile Parapercis colias growth among habitats 21
2.1. Introduction 21
2.2. Methods 23
2.2.1. Habitat surveys and fish collection 23
2.2.2. Differences in length-at-age and weight-at-age among habitats 24
2.2.3. Differences in body condition among habitats 25
2.2.4. Differences in growth rates among habitats 26
2.3. Results 28
2.3.1. Distribution of lengths and weights among habitats 28
2.3.2. Differences in length-at-age and weight-at-age among habitats 29
2.3.3. Differences in body condition among habitats 32

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 2.3.4. Differences in growth rates among habitats 34
2.4. Discussion 39
3. Differences in juvenile Parapercis colias diet among habitats 42
3.1. Introduction 42
3.2. Methods 45
3.2.1. Extraction of prey items from stomachs 45
3.2.2. Differences in feeding opportunities among habitats 45
3.2.3. Differences in prey diversity among habitats 45
3.2.4. Differences in prey abundance among habitats 46
3.2.5. Differences in prey biomass among habitats 46
3.2.6. Changes in diet with increasing juvenile size 47
3.3. Results 48
3.3.1. Differences in feeding opportunities among habitats 48
3.3.2. Differences in prey diversity among habitats 48
3.3.3. Differences in prey abundance among habitats 51
3.3.4. Differences in prey biomass among habitats 55
3.3.5. Changes in diet with increasing juvenile size 59
3.4. Discussion 63
4. Conclusions 66
4.1. Summary of findings 66
4.2. Limitations 66
4.3. Future directions 67
4.4. Management implications 67
References 69

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 List of Figures

1. Introduction
1.1. Bryozoan fields 14
1.2. Dog cockles 15
1.3. Horse mussels 17
1.4. Biogenic clumps 18
1.5. Reef edges 19
2. Differences in juvenile Parapercis colias growth among habitats
2.1. Locations of juvenile P. colias nursery habitats in the Marlborough 24
Sounds, New Zealand
2.2. Section of a polished juvenile P. colias sagittal otolith 27
2.3. Distribution of P. colias lengths in each habitat 28
2.4. Distribution of P. colias weights in each habitat 29
2.5. Length-at-age relationships for juvenile P. colias in each habitat 30
2.6. Weight-at-age relationships for juvenile P. colias in each habitat 31
2.7. Log-transformed length-weight relationship of all juvenile P. colias 32
2.8. Length-weight relationship of all juvenile P. colias with the 33
back-transformed model
2.9. Mean relative condition index of juvenile P. colias in each habitat 34
2.10. Mean growth in length per day of juvenile P. colias in each habitat 35
2.11. Mean growth in weight per day of juvenile P. colias in each habitat 36
2.12. Mean increment width for the full life history of juvenile P. colias in 37
each habitat
2.13. Mean increment width for early and late growth of juvenile P. colias in 38
each habitat
3. Differences in juvenile Parapercis colias diet among habitats
3.1. Number of stomachs that were full or empty in each habitat 48
3.2. Mean species richness of prey found in juvenile P. colias stomachs from 49
each habitat

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3.3. Mean Shannon diversity index of prey found in juvenile P. colias 50
stomachs from each habitat
3.4. Mean species evenness of prey found in juvenile P. colias stomachs 51
from each habitat
3.5. Proportion of prey taxa groups in each habitat 52
3.6. Proportion of prey taxa groups in each habitat with crustaceans and 52
molluscs separated into more specific taxa
3.7. Mean abundance of prey found in the stomachs of juvenile P. colias 53
from each habitat
3.8. Prey taxa where mean abundance was significantly different among 55
habitats
3.9. Proportion of biomass for each prey taxa in each habitat 56
3.10. Proportion of biomass for each prey taxa in each habitat, with 57
crustaceans and molluscs separated into more specific taxonomic groups
3.11. Prey taxa where mean biomass was significantly different among 59
habitats
3.12. Proportions of prey taxa in each juvenile size class for each habitat 61
3.13. Abundance versus length for prey taxa groups where at least one 62
significant relationship was present

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 Chapter 1: Introduction

1.1. Population dynamics and population bottlenecks in fishes

Marine organisms can have complex life histories with distinct larval, juvenile, and adult life
stages (Wilbur, 1980). Success during early life stages is important for population growth for
most fish species (Houde, 1987; Houde, 1997). However, early life stages often suffer from
high rates of mortality because they are extremely vulnerable to biological factors such as
predation (Bailey & Houde, 1989) and diseases (Muroga, 2001), as well as physical factors
such as temperature (Pepin, 1991) and salinity (Bœuf & Payan, 2001). High mortality during
early life stages may have been an evolutionary driving force of the high fecundities observed
in most fish species, a strategy to ensure that more offspring survive to adulthood (Beverton,
1987; Lambert, 2008; Pincheira-Donoso & Hunt, 2017). Early life mortality is one of the
primary drivers of population dynamics in fishes (Houde, 1987; Houde, 1997). Although most
fish species produce many offspring per breeding season, small changes in early life mortality
rates can lead to large changes in population size (Houde, 1987; Houde, 1997). Factors that
act to reduce or limit success during early life stages are called ‘bottlenecks’, which can have
severe consequences for the population (Nei et al., 1975; Ludsin & DeVries, 1997).

1.2. Pre-settlement sources of mortality

Most fish species go through a pelagic larval stage after hatching in the water column, then
undergo metamorphosis into the juvenile and then adult stage (Evans & Fernald, 1990).
Factors such as predation (Anderson, 1998), starvation (Cushing, 1990), and unfavourable
drift (Sinclair, 1988) are the primary sources of mortality during the egg and larval stages, and
act as bottlenecks to population growth. Predation causes direct mortality to individuals when
eggs and larvae are consumed and depends on the abundance and size of predators
(Anderson, 1998; Paradis et al., 1996; Akimova et al., 2019). Starvation occurs when food
availability is low, and often leads to reduced larval growth which hinders the survivability of
individuals (Cushing, 1990; Anderson, 1998). Larval growth depends on the overlap of feeding
larvae with planktonic food, which depends on suitable conditions of temperature and light
(Arula et al., 2015; Doyle et al., 2019). Unfavourable drift often interacts with predation or
starvation, by moving eggs and larvae into areas with conditions more suitable for predators

9
or conditions less suitable for food (Sinclair, 1988). Temperature can also independently lead
to mortality during the larval stage (Pepin, 1991; Muroga, 2001). Most fish species have larvae
with more narrow thermal windows than adults, and do not possess the ability to cope with
heat stress (Pörtner & Peck, 2010). Although some fish species have larvae which can adapt
to abnormal temperatures by regulating proteins related to metabolism, heat stress generally
reduces growth, body condition, fitness, and disease resistance (Madeira et al., 2016).

1.3. Post-settlement sources of mortality

After the pelagic larval stage, most fish species undergo metamorphosis into either a pelagic
or benthic juvenile stage (Evans & Fernald, 1990). Benthic fish species typically have a life
cycle consisting of a pelagic larval stage, followed by a benthic juvenile stage that settles into
biogenic habitats located on the seafloor (Beck et al., 2001; Cheminée et al., 2017). Biogenic
habitats are habitats created by living organisms such as seaweeds, sponges, shellfish, corals,
and plants, that have unique infaunal and epifaunal communities and are often more
productive than soft sediment habitats (Boström et al., 2011; McLeod et al., 2014; Morrison
et al., 2014). Factors such as predation and food availability are still primary sources of
mortality during the juvenile stage (Verweij et al., 2006). However, predation and food
availability depend on habitat characteristics such as the availability of refuges and the
structure of prey communities (Thrush et al., 2002; Carbines et al., 2004; Rogers et al., 2014).
Therefore, the availability of suitable habitats providing sufficient shelter and food for the
juvenile stage can act as a bottleneck to the success of juvenile populations and population
growth (Beck et al., 2001; Nagelkerken et al., 2000; James et al., 2019).

1.4. Juvenile habitats and the role of nurseries

Habitats that provide sufficient shelter and food are important in the success of juvenile
populations and their ability to contribute to population growth (Houde, 1987; Houde, 1997;
Beck et al., 2001). Some juvenile habitats contribute more individuals to the adult population
than others, and often provide significant benefits to juveniles occupying them (Beck et al.,
2001; James et al., 2019). These juvenile habitats are often referred to as a ‘nursery habitat’,
a juvenile habitat that contributes disproportionately more individuals to the adult population
than other habitats on a per unit area basis (Beck et al., 2001). This definition of a ‘nursery
habitat’ can be used to differentiate from an ‘effective juvenile habitat’ (Dahlgren et al.,

10
2006). An effective juvenile habitat is one that does not contribute disproportionately more
individuals to the adult population than other habitats on a per unit area basis, but
contributes more individuals because it has a larger area (Dahlgren, 2006). Specifically, for a
juvenile habitat to qualify as a nursery, it must provide benefits to the abundance, growth,
survival, and recruitment of juveniles to the adult population (Beck et al., 2001; Heck et al.,
2003). Biogenic habitats such as mangroves, seagrass beds, and seaweeds are important
nurseries for juvenile fish species (Dorenbosch et al., 2005; Verweij et al., 2008; Evans et al.,
2014). The quality and value of a nursery depends on the habitat’s ability to provide sufficient
food for growth, as well as refuges that protect juveniles from predators, both of which are
often mediated by habitat complexity (Gratwicke & Speight, 2005; Rogers et al., 2014).
Biogenic habitats can create complex physical structures that increase the availability of
refuges that protect juveniles from predators, and support more diverse, abundant, and
productive prey communities, particularly when compared to soft sediment habitats (McLeod
et al., 2014; Rogers et al., 2014). Habitats with less structural complexity have relatively less
refuges and less diverse, abundant, and productive prey communities, which may hinder the
abundance, growth, and survival of juveniles (Sundblad & Bergström, 2014). The quality and
value of a nursery also depends on the habitat’s proximity and connections to other juvenile
habitats, as well as adult habitats (Sheaves, 2009; Nagelkerken et al., 2015). Juveniles may
not stay in a habitat when food becomes limiting and may migrate to other habitats to
optimize energy spent foraging (Tableau et al., 2016). Furthermore, juveniles may
opportunistically feed in unfavourable habitats while migrating towards more favourable
habitats (James et al., 2019). Juvenile habitats are often also closely connected to adult
habitats, providing safe routes for the recruitment of juveniles to the adult population
(Nagelkerken et al., 2015). This is particularly common in tropical ecosystems, where
mangroves provide a nursery for juvenile fishes before they migrate to coral reefs as adults
(Nagelkerken et al., 2000; Mumby et al., 2004).

1.5. Anthropogenic impacts on nurseries

For centuries, anthropogenic activities have significantly changed the structure and function
of marine ecosystems, particularly those located in coastal waters, where a wide range of
biogenic habitats are located (Jackson et al., 2001). Coastal ecosystems are under immense
pressure from anthropogenic activities such as shellfish dredging, bottom trawling, and

11
coastal development (Riemann & Hoffmann, 1991; Ralph et al., 2007; Dolbeth et al., 2011).
These activities have severe consequences for biogenic habitats and their ability to provide
nurseries for many fish species, creating a significant bottleneck to the success of juvenile
populations and therefore population growth (Rochette et al., 2010; Carugati et al., 2018;
Rogers & Mumby, 2019). Fishing activities such as shellfish dredging and bottom trawling can
cause direct fatal damage to biogenic habitats and their associated infaunal and epifaunal
communities (Riemann & Hoffmann, 1991). Sedimentation from fishing activities and coastal
development can smother biogenic habitats and hinder their recovery by creating a loose
substrate that prevents the attachment of propagules (Wilber & Clarke, 2001; Erftemeijer et
al., 2012). Toxic contaminants from urban runoff can have lethal effects on biogenic habitats
and their faunal communities (Roberts et al., 2008).

1.6. Parapercis colias in the Marlborough Sounds, New Zealand

The loss of nursery habitats can have significant consequences for fishery species (Morrison
et al., 2009; Sundblad et al., 2014; Rogers & Mumby, 2019). Many of New Zealand’s most
important fishery species rely on biogenic habitats such as kelp forests and seagrass beds, for
rearing juveniles (Willis & Anderson, 2003; Morrison et al., 2009; Morrison et al., 2014).
Parapercis colias, also known as ‘blue cod’ or ‘rāwaru’, are an important commercial and
recreational fishery species found mostly around the South Island of New Zealand (Cranfield
et al., 2001; MPI, 2021). P. colias eggs are pelagic for approximately five days, and larvae are
pelagic for additionally five more days, before settling into habitats located on the seafloor
(MPI, 2021). Juveniles and adults spend most of their lifetime on the benthos, where they
depend on biogenic habitats such as shellfish beds, bryozoan fields, and sponge gardens for
food and protection from predators (Cranfield et al., 2001; Jiang & Carbines, 2002; Carbines
et al., 2004; Morrison et al., 2014). Like other fish species, P. colias are highly susceptible to
sources of mortality such as predation and starvation during early life stages (Cushing, 1990;
Verweij et al., 2006). The Marlborough Sounds is an extensive network of rias or drowned
valleys containing biogenic habitats and has been a popular commercial and recreational
fishing ground for P. colias since the early 1900s (Nicol, 2011; MPI, 2021). The region has also
been a popular fishing ground for scallops, which are commercially caught via dredging
(Williams et al., 2019; MPI, 2021). It is possible that commercial bottom trawling and shellfish
dredging activities have caused damage to P. colias habitat (Cranfield et al., 2001; Carbines et

12
al., 2004). Although interactions between adult P. colias and their habitat have been observed
in previous studies (Cranfield et al., 2001; Jiang & Carbines, 2002; Carbines et al., 2004),
juvenile habitat associations have been rarely explored (Mutch, 1983). Furthermore, no
studies have explored the qualities of P. colias nursery habitats and what makes them
valuable to juveniles.

1.7. Parapercis colias nurseries in the Marlborough Sounds, New Zealand

Regional-scale surveys of the Marlborough Sounds, conducted in 2017 and 2019 by the
National Institute of Water and Atmospheric Research (NIWA) research programme ‘Juvenile
fish habitat bottlenecks’, CO1X618, funded by Ministry of Business, Innovation and
Employment (MBIE), assessed the composition of habitats located on the seafloor. Towed
video cameras with scaling lasers were used to assess habitat characteristics, measure the
densities and sizes of juvenile P. colias and other fish species, and identify nursery habitats
for P. colias. Five different habitat types were identified: bryozoan fields, dog cockle beds,
horse mussel beds, biogenic clumps, and reef edges.

1.7.1. Bryozoan fields

New Zealand waters are a global hotspot for bryozoans, with over 1000 known species (Wood
et al., 2012). About 50 of these species are defined as ‘frame builders’, which are species that
grow large enough to be classified as biogenic habitats (Wood et al., 2012). Bryozoans are
often associated with other habitat-forming species such as sponges, and harbour rich and
abundant communities of small invertebrates (Morrison et al., 2014). In the Marlborough
Sounds, bryozoan fields are much rarer in the present day, and historical accounts suggest
that they were once more widespread (Bradstock & Gordon, 1983; Morrison et al., 2014).
Juvenile P. colias have been previously observed occupying bryozoan fields off the Otago
Peninsula (Jones et al., 2016), and in Foveaux Strait (Carbines & Cole, 2009).

13
Figure 1.1. Bryozoan fields with Cinctipora elegans, sponges, ascidians, starfish, and red algae.

1.7.2. Dog cockle beds

The large dog cockle Tucetona laticostata is a common bivalve found in New Zealand,
occurring in shallow waters and up to depths of 80 m on the continental shelf (Morrison et
al., 2014). Dog cockle beds often occur in areas with relatively coarse sediment and high
current flow (Morrison et al., 2014). Shells often form drifts on the seafloor which enhance
densities of small invertebrate communities and provide a substrate for the attachment of
other habitat-forming species such as bryozoans, sponges, and macroalgae (Dewas & O’Shea,

14
2012). In the Marlborough Sounds, dog cockle beds typically occur in high current flow
channels between islands and off rocky promontories, with current speeds and coarse
sediments likely structuring their distribution (Morrison et al., 2014). Dog cockle beds often
do not occur in open soft sediment areas (Morrison et al., 2014). Juvenile P. colias have been
previously observed occupying dead shell drifts (Carbines et al., 2004).

Figure 1.2. Dog cockle beds with small rocks and red calcareous algae.

15
1.7.3. Horse mussel beds
The horse mussel Atrina zelandica is also a common bivalve found in New Zealand, occurring
at the low tide mark up to depths of 100 m on the continental shelf (Morrison et al., 2014).
Horse mussels typically sit upright and half-buried in the seafloor, being held in place by
bysuss threads (Morrison et al., 2014). Horse mussels can form dense and extensive beds, and
often provide a substrate for the attachment of other species such as bryozoans, sponges,
and macroalgae (Morrison et al., 2014). In the Marlborough Sounds, horse mussel beds have
been significantly impacted by sedimentation, bottom trawling, and scallop dredging, which
have directly damaged beds and reduced their ability to support epifaunal communities and
fish assemblages (Hay, 1990). Horse mussel beds in northern New Zealand are important
nursery habitats for juvenile Pagrus auratus (Compton et al., 2012), and juvenile P. colias have
also been previously observed to occupy horse mussel beds (Mutch, 1983).

16
Figure 1.3. Horse mussel beds with attached Cinctipora elegans, brittle stars, sea cucumbers,
and filamentous red algae.

1.7.4. Biogenic clumps

Biogenic habitats are often created by a mixture of different habitat-forming species, with no
particular species being more dominant than others (Morrison et al., 2014). In the
Marlborough Sounds, clumps of habitat-forming species, or ‘biogenic clumps’, primarily
include combinations of bryozoans, dog cockles, horse mussels, sponges, hydroids, and
macroalgae, which support a diverse array of infaunal and epifaunal communities (Morrison

17
et al., 2014). Juvenile P. colias have been observed occupying biogenic clumps found in the
Marlborough Sounds (Morrison et al., unpublished data).

Figure 1.4. Biogenic clumps consisting of various sponges, bryozoans, red macroalgae, and
shellfish.

1.7.5. Reef edges

Most of the Marlborough Sounds and associated islands are fringed with relatively narrow
reefs that merge with the adjacent soft sediment seafloor close to land (Morrison et al., 2014).

18
These reefs are often fringed by a narrow zone mixed with cobbles or biogenic material
composed of dead carbonate debris such as mollusc shells and calcareous tubeworms
(Morrison et al., 2014). Juvenile P. colias have been observed occupying reef edges in the
Marlborough Sounds (Morrison et al., unpublished data).

Figure 1.5. Reef edges consisting of dead calcareous debris.

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1.8. Thesis aims
In this thesis, I assessed the quality and value of juvenile P. colias nursery habitats by
quantifying and comparing growth and diet among 5 different nursery habitat types
(bryozoan fields, dog cockle beds, horse mussel beds, biogenic clumps, and reef edges), to
identify the best nursery habitat(s) for P. colias. In Chapter 2, I quantified and compared
growth patterns, body condition, and growth rates of juvenile P. colias captured from each
habitat type. In Chapter 3, I analysed stomach contents from the same fish to compare diets
among habitats, focusing on differences in the diversity, abundance, and biomass of prey.

20
 Chapter 2: Differences in juvenile Parapercis colias growth among habitats

2.1. Introduction

Marine organisms can have complex life histories with distinct larval, juvenile, and adult life
stages (Wilbur, 1980). Environmental conditions can affect the growth of individuals during
any life stage, which can have flow-on effects on fitness and survival in later stages
(Mortensen et al., 2000; Shima & Findlay, 2002). Growth is defined as an increase in size via
the synthesis of new tissues, given the sufficient consumption of food (Shreck & Moyle, 1990).
Marine fishes generally have indeterminate growth, where they continue to grow after
reaching maturity and throughout their lives (Charnov & Berrigan, 1991). Although genetics
has key roles in pre-determining growth, environmental factors such as food consumption
and temperature can have greater influences on growth during early life stages, and can lead
to intraspecific variation in growth when individuals are living under different conditions
(Jones, 1986; Pepin, 1991; Bradbury et al., 2010).

Several physical properties such as temperature (Pepin, 1991), turbidity (Fiksen et al., 2002),
salinity (Bœuf & Payan, 2001), oxygen concentration (Mallya, 2007), photoperiod (Trippel &
Neil, 2003), and lunar rhythms (Shima et al., 2021) can influence growth in fishes. Physical
factors have independent effects but are often connected and interact with each in the
marine environment (Gunderson et al., 2016). Physical factors also interact with biological
factors such as predation (Ferrari et al., 2015), food availability (Korman et al., 2021),
competition (Kordas et al., 2011), and the provision of biogenic habitats (Pratchett et al.,
2008; Blain & Shears, 2019).

Biogenic habitats are habitats created by living organisms such as seaweeds, sponges,
shellfish, corals, and plants, and often have unique faunal communities and physical
structures that enhance growth in fishes (Boström et al., 2011; Morrison et al., 2014). Infaunal
and epifaunal communities living inside and on the surface of biogenic structures and the
surrounding seafloor are an important food source for fishes (Connolly, 1994). Furthermore,
refuges created by biogenic structures provide protection from predators (Rogers et al.,

21
2014). Food and refuge availability can influence growth and survival, where habitats with
more food and refuges support faster growing individuals that spend less time at a vulnerable
size to predators, and larger individuals that are less susceptible to predation (Anderson,
1988; Hixon & Beets, 1993). The provision of food and refuges in biogenic habitats is
particularly important for fish species that have a benthic juvenile stage (Verweij et al., 2006).

Parapercis colias are an important fish species in New Zealand, with significant value as a
commercial and recreational fishery (MPI, 2021). P. colias have a benthic juvenile stage, and
adults are heavily reliant on food and shelter provided by biogenic habitats located on the
seafloor for growth (Jiang & Carbines, 2002; Carbines et al., 2004). However, no studies have
explored juvenile growth in biogenic habitats, and whether growth varies among different
habitat types.

Growth in fishes is typically quantified using a combination of length, weight, and age (Shreck
& Moyle, 1990). Otoliths are the most commonly used structure for age determination in fish
(Popper & Lu, 2000). Generally found in teleost fish, otoliths are small calcareous structures
primarily used for hearing (Popper & Lu, 2000). Most fish usually have three different pairs of
otoliths: sagittae, lapilli, and asterisci, all located in the inner ears (Popper & Lu, 2000). Sagittal
otoliths are the most popular type of otolith used in aging studies, and have been extensively
used by fisheries scientists to study annual growth in adult P. colias (Walsh, 2017). However,
otoliths have never been used to study daily growth in juvenile P. colias, nor have they been
used to study relationships between juvenile P. colias growth and their habitat.

In this chapter, I investigated relationships between juvenile P. colias growth and habitat type,
to assess the quality and value of juvenile P. colias nursery habitats. I used daily growth
increments found in the sagittal otoliths of juvenile P. colias to evaluate variation in growth
among 5 different nursery habitats (biogenic clumps, bryozoans, dog cockles, horse mussels,
and reef edges). Specifically, I addressed three questions: (1) Do juvenile length-at-age and
weight-at-age relationships differ among habitats? (2) Does juvenile body condition differ
among habitats? (3) Do juvenile growth rates differ among habitats?

22
2.2. Methods

2.2.1. Habitat surveys and fish collection

All samples used in this research were collected as part of a regional-scale survey of the
Marlborough Sounds, conducted by the National Institute of Water and Atmospheric
Research (NIWA) research programme ‘Juvenile fish habitat bottlenecks’, CO1X1618, funded
by Ministry of Business, Innovation and Employment (MBIE). Sampling sites were selected to
represent a range of juvenile P. colias nursery and non-nursery habitats, based on earlier
large-scale surveys of the Marlborough Sounds in 2017 and 2019. Towed video cameras with
scaling lasers were used to assess habitat characteristics and measure the densities and sizes
of juvenile P. colias and other fish species. Twenty sites geographically spread as wide as
possible were selected for sampling in 2019 covering five juvenile habitat types: biogenic
clumps (3 sites), bryozoan fields (2 sites), dog cockle beds (2 sites), horse mussel beds (3), and
reef edges (10) (Figure 2.1). Juvenile P. colias were collected from each site between April
2019 and May 2019, by divers armed with multi-pronged spearguns. Onboard the research
vessel, fish fork lengths (mm) were measured, guts were dissected out and injected with 10%
formalin for preservation, and the remainder of the body was frozen for the later
measurement of gutted weight (g) and the removal of otoliths at NIWA, Auckland. Habitat
seafloor samples were also collected by divers. Depending on the characteristics of the
habitat being sampled, parts of the habitat were collected from each site via hand-cores,
enclosing bags, or battery-powered suction samplers. Habitat samples will be used for the
analysis of prey assemblages, not examined in this thesis.

23
Figure 2.1. Locations of potential juvenile P. colias nursery habitats in the Marlborough
Sounds, New Zealand. Juveniles were found in sites labelled red. Sites labelled in green were
also surveyed but did not have any juveniles present and were classified as non-nursery
habitats.

2.2.2. Differences in length-at-age and weight-at-age among habitats

To test whether length-at-age and weight-at-age relationships of juvenile P. colias differed
among habitats, the age of each juvenile had to be determined. Otoliths were processed from
June 2020 to December 2020 at the Wellington University Coastal Ecology Lab (WUCEL). Each
otolith was first cleaned in distilled water, then embedded in a thermoplastic adhesive

24
(Crystalbond) and affixed to an acrylic disc with the sulcus side of the otolith facing up. The
sulcus side was polished by hand on wet 9 µm and 3 µm diamond lapping films until the
nucleus was visible at 100X magnification. The adhesive was reheated, and the otolith was
flipped over so that the non-sulcus side was facing up. Polishing was repeated on the non-
sulcus side of the otolith using wet 9 µm and 3 µm diamond lapping films until daily growth
increments were clearly visible at 100X magnification along the whole counting axis. A thin
layer of adhesive was added to the surface of the otolith to improve the clarity of increments.
The embedded otoliths were left to set for 24 hours. Before imaging, a drop of immersion oil
was placed on the surface of each otolith to further improve the clarity of increments. The
non-sulcus side of each otolith was photographed with a camera attached to a compound
microscope (Leica DM2500) set at 100X magnification, which was enough to discern daily
growth increments. However, at this magnification level, the full counting axis could not be
captured in a single image, therefore multiple images were taken along the whole counting
axis and combined using the stitching tool in Leica Application Suite (Figure 2.2) (version 4.3).
Otolith images were analysed using the Otolith M application in Image-Pro Premier (version
9.3). Daily growth increments were marked and counted from the otolith edge to the core.
Increments were marked on a single axis line in order to record increment widths for further
analysis involving growth rates. When increments did not appear clearly on the axis line, the
area around the counting axis was used to decide on whether an increment was present or
not. To ensure that increment width measurements were as accurate as possible, the specific
location of these increments on the axis line was visually estimated using the visual widths of
surrounding increments. All statistical analyses were conducted in R (version 4.0.3) at the 5%
significance level. Linear regression was used to test the presence of length-at-age and
weight-at-age relationships in each habitat, and analysis of covariance (ANCOVA) was used to
test the interactive effects of habitat and age (covariate) on length and weight.

2.2.3. Differences in body condition among habitats

To determine whether the body condition of juvenile P. colias differed among habitats, a
relative condition index (RCI) (Francis, 1997) was calculated for each fish by dividing the
observed weight by the expected weight and subtracting 1 (RCI = Observed weight/Expected
weight – 1) to make normal body condition a value of 0. The expected weight was calculated
using the length-weight relationship equation: 𝑊 = 𝑎𝐿! , where W is the expected weight, a

25
is a constant and scaling coefficient for the weight at length, L is the measured length, and b
is a parameter for body shape and the type of growth. Growth parameters were estimated
by maximum likelihood estimation, from a model fit to all fish (n = 309) using the nls function
in R (version 4.0.3). However, the model showed unequal variances, with the residuals
‘funnelling’ or becoming greater at higher values of length and weight. For this reason, I log-
transformed the data and fitted a linear model using the lm function in R (version 4.0.3). The
RCI looks at the differences between observed and expected weights, or the residuals
between the data and model fit. A value of 0 represents expected or normal body condition,
while values above (better) or below (worse) 0 show deviations from normal. An analysis of
variance (ANOVA) was conducted in R (version 4.0.3) at the 5% significance level to compare
the average RCI among habitats.

2.2.4. Differences in growth rates among habitats

To determine whether juvenile P. colias growth differed among habitats, three different
measurements were used to estimate growth rates: lengths (mm), weights (g), and otolith
daily increment widths (µm). Growth rates were inferred from length/age, weight/age, and
increment widths. For otolith increments, the average width between all daily increments
was calculated to capture growth for the full life history of each fish. Additionally for each
fish, late growth was calculated by averaging the widths of the first 50 increments from the
otolith edge, and early growth was calculated by averaging the widths of the next 50
increments. Only otoliths with at least 110 daily growth increments were used in analyses of
increment width, to capture both early and late growth with 50 increments each. All statistical
analyses were conducted in R (version 4.0.3) at the 5% significance level. ANOVA was used to
compare growth rates inferred from length/age, weight/age, and increment width (full, early,
and late) among habitats.

26
Figure 2.2. Section of a polished juvenile P. colias sagittal otolith created by stitching together
multiple images of sections viewed under a compound microscope at 100X magnification.

27
2.3. Results

2.3.1. Distribution of lengths and weights among habitats

Lengths of juvenile P. colias (n = 309) ranged from 46 to 108 mm (Mean = 85.5, SD = 12.2),
and weights from 0.82 to 15.45 g (Mean = 7.04, SD = 2.79). The reef edge habitat covered the
widest distribution of length (Figure 2.3) and weight (Figure 2.4) classes compared to all other
habitats.

70

60

50
Frequency

40
Reef Edge
30 Horse Mussels
Dog Cockles
20
Bryozoans
10 Biogenic Clumps

0
45-49

50-54

55-59

60-64

65-69

70-74

75-79

80-84

85-89

90-94

95-99

100-104

105-109

Length class (mm)

Figure 2.3. Distribution of juvenile P. colias lengths in each habitat.

28
 60

50

40
Frequency

Reef Edge
30
Horse Mussels
Dog Cockles
20
Bryozoans
10 Biogenic Clumps

0
0-1
1-2
2-3
3-4
4-5
5-6
6-7
7-8
8-9
9-10
10-11
11-12
12-13
13-14
14-15
15-16
Weight class (g)

Figure 2.4. Distribution of juvenile P. colias weights in each habitat.

2.3.2. Differences in length-at-age and weight-at-age among habitats

Out of the 309 otoliths processed, 184 had daily growth increments visible along the full
counting axis, while 125 had large areas where increments were not visible due to breaking
or over-polishing. Only otoliths with the whole counting axis present were used for further
age analysis. Ages of juvenile P. colias (n = 184) ranged from 53 to 240 days old (Mean = 164.8,
SD = 30.1). Length significantly increased with age for juveniles in all habitats: biogenic clumps
(R2 = 0.29, F1, 15 = 6.097, p = 0.026), bryozoans (R2 = 0.73, F1, 12 = 33.15, p < 0.001), dog cockles
(R2 = 0.42, F1, 36 = 25.93, p < 0.001), horse mussels (R2 = 0.17, F1, 37 = 7.561, p = 0.009), and reef
edges (R2 = 0.76, F1, 74 = 231.4, p < 0.001). When testing for the interactive effect of age and
habitat on length, a significant interaction was found (F4, 174 = 2.654, p = 0.03), indicating that
the effect of age on length depends on the habitat type (Figure 2.5).

29
 120

100
Length (mm)

Biogenic Clumps
80 Bryozoans
Dog Cockles
Horse Mussels
60
Reef Edge

40
0 50 100 150 200 250
Age (days)

Figure 2.5. Length-at-age relationships for juvenile P. colias in each habitat. Length-at-age
equations were: biogenic clumps (Length = 42.27 + 0.24*Age), bryozoans (Length = 35.59 +
0.29*Age), dog cockles (Length = 48.62 + 0.22*Age), horse mussels (Length = 58.07 +
0.16*Age), and reef edges (Length = 35.50 + 0.32*Age).

Weight significantly increased with age for juveniles in bryozoans (R2 = 0.66, F1, 12 = 23.74, p <
0.001), dog cockles (R2 = 0.35, F1, 36 = 19.07, p < 0.001), horse mussels (R2 = 0.15, F1, 37 = 6.55,
p = 0.014), and reef edges (R2 = 0.64, F1, 74 = 128.8, p < 0.001), but not biogenic clumps. When
testing for the interactive effect of habitat and age on weight, no significant interaction was
found, but the main effect of habitat was significant (F4, 174 = 9.874, p < 0.001). Post hoc
analyses (Tukey’s test) showed that juveniles from reef edges were generally heavier than
juveniles from all other habitats at all ages (Figure 2.6).

30
 16

14

12

10
Weight (g)

Biogenic Clumps
8 Bryozoans
Dog Cockles
6
Horse Mussels
4
Reef Edge
2

0
0 50 100 150 200 250
Age (days)

Figure 2.6. Weight-at-age relationships for juvenile P. colias in each habitat. Weight-at-age
equations were: bryozoans (Weight = -2.04 + 0.051*Age), dog cockles (Weight = -1.26 +
0.049*Age), horse mussels (Weight = 0.98 + 0.033*Age), and reef edges (Weight = -3.08 +
0.067*Age).

Due to the reef edge habitat having more young and small juveniles than other habitats, it is
possible that the linear models for reef edges were skewed more towards lower values than
other habitats. To explore this bias, I repeated all analyses using only juveniles at or above
110 days old. For length, a significant positive relationship between the length and age of
juveniles was still found in all habitats. However, there was no interactive effect of habitat
and age on length. The main effect of habitat was significant (F4, 164 = 6.219, p < 0.001), and
post hoc analyses (Tukey’s test) showed that juveniles from reef edges were generally longer
than juveniles from dog cockles and horse mussels at all ages. For weight, a significant positive
relationship between the weight and age of juveniles was still found in dog cockles, horse
mussels, and reef edges, but not biogenic clumps or bryozoans. Similar to when using the full
age range, there was no interactive effect of habitat and age on weight, but the main effect
of habitat was significant (F4, 164 = 11.15, p < 0.001). Post hoc analyses (Tukey’s test) showed
that juveniles from reef edges were generally heavier than juveniles from all other habitats
at all ages.

31
2.3.3. Differences in body condition among habitats
When calculating the expected weight of each fish for the RCI, the length-weight model
showed unequal variances, with the residuals ‘funnelling’ or becoming greater at higher
values of length and weight. For this reason, I log-transformed the data and fitted a linear
model to calculate expected weight and the RCI. Figure 2.7 shows the fitted linear model and
Figure 2.8 shows the back-transformed non-linear model.

Figure 2.7. Log-transformed length-weight relationship (R2 = 0.97, F1, 307 = 9990, p < 0.001)
with the equation: Log expected weight = -2.66 + 3.35*Log length.

32
Figure 2.8. Length-weight relationship of all juvenile P. colias with the back-transformed
model.

Juvenile P. colias from bryozoan, dog cockle, and reef habitats had an average RCI above 0,
while juveniles from biogenic clump and horse mussel habitats had an average RCI below 0.
The average RCI of juvenile P. colias was significantly higher in reef edge habitats than in
biogenic clump and horse mussel habitats (F4, 304 = 5.987, p < 0.001). Post hoc analyses
(Tukey’s test) showed that the average RCI in reef edge habitats was 0.007 higher than in
biogenic clump habitats, and 0.006 higher than in horse mussel habitats (Figure 2.9).

33
 0.008

ab b
0.004 ab
Relative condition index

0
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
a a

-0.004

-0.008
Habitat

Figure 2.9. Mean relative condition index (± SE) of juvenile P. colias in each habitat. Lowercase
letters denote groups with similar means.

Similar to previous analyses, the reef edge habitat having more young and small juveniles
than other habitats could have possibly had an effect on RCI values. I therefore repeated the
analyses using only juveniles at or above 110 days old. In this case, juveniles from bryozoans,
dog cockles, and reef edges had an average RCI above 0, while juveniles from biogenic clumps
and horse mussels had an average RCI below 0. However, the average RCI of juveniles was
not only higher in reef edges than biogenic clumps and horse mussels, but also higher in
bryozoans than biogenic clumps and horse mussels (F4, 294 = 6.49, p < 0.001).

2.3.4. Differences in growth rates among habitats

Growth rate estimated as length (mm)/age (days), was significantly higher in juvenile P. colias
from reef edge habitats than juveniles from bryozoan and dog cockle habitats (F4, 179 = 4.163,
p = 0.003). Post hoc analyses (Tukey’s test) showed that juveniles from reef edges grew an
average 0.065 mm more in length per day than juveniles from bryozoans, and 0.047 mm more
than juveniles from dog cockles (Figure 2.10).

34
 0.6

Mean length (mm) per day b

ab
0.55
a
ab
a

0.5

0.45
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 2.10. Mean growth in length per day (± SE) of juvenile P. colias in each habitat.
Lowercase letters denote groups with similar means.

Growth rate estimated as weight (g)/age (days), was significantly higher in juvenile P. colias
from reef edge habitats than juveniles from biogenic clump and horse mussel habitats (F4, 179
= 5.348, p < 0.001). Post hoc analyses (Tukey’s test) showed that juveniles from reef edges
grew an average 0.013 g more in weight per day than juveniles from biogenic clumps, and
0.007 g more than juveniles from horse mussels (Figure 2.11).

35
 0.05
b
Mean weight (g) per day

0.045 ab
a
ab

0.04

0.035

0.03
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 2.11. Mean growth in weight per day (± SE) of juvenile P. colias in each habitat.
Lowercase letters denote groups with similar means.

Daily growth increment widths (µm) in otoliths (age ³ 110 days) over the full life history was
significantly higher in juvenile P. colias from dog cockle, horse mussel, and reef edge habitats
than in juveniles from both biogenic clump and bryozoan habitats (F4, 169 = 10.35, p < 0.001).
Post hoc analyses (Tukey’s test) showed that increments were an average 0.52 µm wider in
juveniles from dog cockles, 0.59 µm wider in juveniles from horse mussels, and 0.57 µm wider
in juveniles from reef edges than in juveniles from biogenic clumps. Increments were an
average 1.00 µm wider in juveniles from dog cockles, 1.07 µm wider in juveniles from horse
mussels, and 1.05 µm wider in juveniles from reef edges than in juveniles from bryozoans
(Figure 2.12).

36
 6
b
Mean increment width (µm) b b

5.5 a

5 a

4.5

4
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 2.12. Mean increment width for the full life history of juvenile P. colias (± SE) in each
habitat. Lowercase letters denote groups with similar means.

Early growth increment width (µm) was significantly higher in juveniles from reef edges than
in juveniles from bryozoans (F4, 169 = 3.163, p = 0.015). Specifically, post hoc analyses (Tukey’s
test) showed that increments were an average 0.80 µm wider in juveniles from reef edges
than juveniles from bryozoans (Figure 2.13). Late growth increment width (µm) was
significantly higher in juveniles from dog cockles and horse mussels than juveniles from
bryozoans (F4, 169 = 4.421, p = 0.002). Post hoc analyses (Tukey’s test) showed that increments
were an average 0.84 µm wider in juveniles from dog cockles than juveniles from bryozoans,
and 1.05 µm wider in juveniles from horse mussels than juveniles from bryozoans (Figure
2.13).

37
 6.5

Mean increment width (µm) 6 ab ab ab b

a
5.5
b b
5 ab ab

4.5 Early
a
Late
4

3.5

3
Biogenic Bryozoans Dog Cockles Horse Mussels Reef Edge
Clumps
Habitat

Figure 2.13. Mean increment width (± SE) for early (50 days) and late growth (50 days) of
juvenile P. colias in each habitat. Lowercase letters denote groups with similar means.

Similar to previous analyses, the reef edge habitat having more young and small juveniles
than other habitats could have possibly had an effect on the growth rates estimated as length
per day and weight per day. I therefore repeated the analyses using only juveniles at or above
110 days old. Growth rate estimated as length per day was not significantly different among
habitats. Growth rate estimated as weight per day was significantly higher in juveniles from
reef edges than in juveniles from biogenic clumps, dog cockles, and horse mussels (F4, 169 =
11.06, p < 0.001).

38
2.4. Discussion

Juvenile P. colias showed significant differences in growth among habitats, demonstrating the
importance of habitat type in juvenile growth. Comparisons of length-at-age relationships
among habitats showed an interactive effect of age and habitat on length, where the effect
of age on length depends on the habitat type. Juveniles from reef edges were typically smaller
at a young age compared to juveniles from other habitats, but were larger than juveniles from
other habitats at an old age. However, reef edges also had notably more young and small
juveniles than other habitats, skewing the linear model for reef edges more towards lower
values than other habitats. When I repeated the analyses using only juveniles at or above 110
days old, the interactive effect of age and habitat on length was no longer present, but the
significant main effect of habitat showed that juveniles from reef edges were typically larger
than juveniles from dog cockles and horse mussels at all ages. Comparisons of weight-at-age
relationships among habitats did not show an interactive effect of age and habitat on length.
Juveniles from reef edges were typically heavier than juveniles from other habitats at all ages
and analyses using only juveniles at or above 110 days old showed the same results. My
comparisons of length-at-age and weight-at-age suggest better juvenile growth in reef edges.

Comparisons of body condition among habitats showed that juveniles from bryozoans, dog
cockles, and reef edges were in significantly better condition, weighing relative more than
their normal expected weight. Juveniles from biogenic clumps and horse mussels were in
significantly worse condition, weighing relatively less than their normal expected weight.
Additionally, juveniles from reef edges were in significantly better condition than juveniles
from biogenic clumps and horse mussels. Furthermore, analyses using only juveniles at or
above 110 days old showed that juveniles from bryozoans were also in significantly better
condition than juveniles from biogenic clumps and horse mussels. My comparisons of body
condition provided further evidence for better juvenile growth in reef edges, but also
highlighted the importance of bryozoans in facilitating growth.

Comparisons of growth rates inferred from length/age showed that juveniles from reef edges
grew significantly larger per day than juveniles from bryozoans and dog cockles. Comparisons
of growth rates inferred from weight/age showed that juveniles from reef edges gained

39
significantly more weight per day than juveniles from biogenic clumps and horse mussels.
Comparisons of growth rates inferred from daily growth increment widths over the full life
history showed that juveniles from dog cockles, horse mussels, and reef edges grew
significantly faster per day than juveniles from biogenic clumps and bryozoans. Late growth
inferred from widths of the first 50 daily increments from the otolith edge showed that
juveniles from dog cockles and horse mussels grew significantly faster per day than juveniles
from bryozoans. Early growth inferred from widths of the next 50 daily increments showed
that juveniles from reef edges grew significantly faster per day than juveniles from bryozoans.
My comparisons of growth rates inferred from lengths, weights, and increment widths
provided even further evidence for better juvenile growth in reef edges, but showed slower
growth in bryozoans.

My results showed strong evidence for faster juvenile P. colias growth in reef edges,
suggesting that reef edge habitats in the Marlborough Sounds provide better conditions for
juvenile growth. This could be due to many different factors such as relatively increased food
availability, refuge availability, or swimming efficiency compared to other habitats (Jones,
1986; Roche et al., 2014; Rogers et al., 2014). The presence of more food and refuges can
support faster growing fish that spend less time at vulnerable sizes to predators, and larger
fish that are less susceptible to predation (Anderson, 1988; Hixon & Beets, 1993). Energy
demands for movement depend on water flow and the activity required to hold an efficient
position in the water column (Roche et al., 2014). Relatively large physical structures created
by biogenic habitats can reduce water flow to an optimum level that distributes sufficient
amounts of nutrients and minimises energy demands for movement (Parsons et al., 2015).
This can significantly aid in foraging activities, allowing individuals to live in habitats with a
high flow of nutrients that support their prey (Parsons et al., 2018). Reef edges in the
Marlborough Sounds are primarily made up of cobble and dead calcareous material such as
mollusc shells (Figure 1.5). Although the source of the shells is unknown, it is likely that they
have drifted from nearby shellfish beds which require a high flow of nutrients (Clausen &
Riisgård, 1996). Dense beds of cobble and shells could additionally be creating structurally
complex habitats that support more productive prey communities, reduce the vulnerability
of juveniles to predators by providing refuges, and reduce energy spent on movement
(Gratwicke & Speight, 2005; Kovalenko et al., 2012; McLeod et al., 2014). It is possible that

40
reef edges are more complex in structure than other habitats, although this would need to be
tested further by examining the physical structure of each habitat.

This research highlighted the importance of habitat type in the growth of juvenile P. colias,
suggesting that the quality and value of different nursery habitats varies. Knowledge of the
mechanisms driving differences in juvenile growth are important in furthering our
understanding of what qualities make particular nursery habitats more valuable than others.
In Chapter 3, I explored one of these mechanisms, by investigating differences in juvenile P.
colias diets among the same nursery habitats.

41
 Chapter 3: Differences in juvenile Parapercis colias diet among habitats

3.1. Introduction

Predator-prey interactions describe biological interactions between predator species and

prey species, and are a major driver of predator populations, prey populations and ecosystem
dynamics in the marine environment (Lima, 1998; Fauchald et al., 2000). The success of
predator populations depends on their ability to capture prey, while the success of prey
populations depends on their ability to avoid predators and develop behavioural or
morphological mechanisms to avoid capture (Fauchald et al., 2000; Benoit-Bird & Au, 2003).
Fishes are some of the most common predators in the marine environment and often possess
complex behavioural and morphological adaptations that influence predator-prey dynamics
(Rahel & Stein, 1988). Knowledge of the foraging strategies and diets of fish are important for
understanding predator-prey interactions, particularly how predator populations respond to
changes in prey populations (Adams et al., 1982; Graeb et al., 2004).

Several physical factors such as photoperiod (Kaartvedt & Titelman, 2018), temperature
(Murphy et al., 2013), turbidity (Sohel et al., 2017), oxygen concentation (Taylor & Eggleston,
2000), salinity (Schallenberg et al., 2003), and moonlight (Shima & Swearer, 2019) can
influence predator-prey interactions and changes in prey populations. Physical factors are
particularly important in maintaining the health of epifaunal and infaunal communities found
in biogenic habitats, which are habitats created by living organisms such as seaweeds,
sponges, shellfish, corals, and plants (Morrison et al., 2014; Sheehan et al., 2015). Epifaunal
and infaunal communities living on the surface and inside biogenic structures and the
surrounding seafloor are an important source of food for fishes (Connolly, 1994; McLeod et
al., 2014). Variability in the diversity of prey communities found among different biogenic
habitats can lead to intraspecific variation in predator-prey interactions, foraging strategies,
diets, and growth when individuals are living in different habitats (Heck & Crowder, 1991;
Thrush et al., 2002). This is particularly important for benthic fish species that occupy a range
of different habitats (Jiang & Carbines, 2002; Thrush et al., 2002; Szedlmayer & Lee, 2004).

42
Knowledge of the feeding strategies and diets of benthic fish species is critical for
understanding the importance of biogenic habitats, the importance of prey communities, and
the value of certain prey species (Schafer et al., 2002; Nagelkerken & Van der Velde, 2004;
Tse et al., 2018). Feeding strategies can predict the impact of different prey communities
among different habitats (Hempson et al., 2017). Generalist feeders are not restricted to any
specific type of food, consume a wide variety of prey, can switch prey in response to
availability, and are therefore adapted to survive in various environments with different prey
communities (Costello, 1990; Laske et al., 2018). Specialist feeders have more restricted diets
and are adapted to capture more specific prey, but are less adapted to survive when
conditions and prey communities change (Costello, 1990; Vanderpham et al., 2013). Although
feeding strategies influence the ability for species to survive among different habitats with
different prey communities, the nutritional value of prey species varies and depends on the
dietary requirements of predators (Shreck & Moyle, 1990; Brooker et al., 2013).

Nutrients such as proteins, carbohydrates, lipids, vitamins, and minerals are all essential in
the diets of fishes, and contribute to healthy growth, body condition, fitness, and movement
(Shreck & Moyle, 1990; Halver, 2013). Each type of nutrient serves a unique purpose in
physiological functions (Shreck & Moyle, 1990; Halver, 2013). Prey species can differ in
nutritional content, with some being more valuable than others for certain predators (Duffy
& Paul, 1992; Brooker et al., 2013). This could lead to intraspecific variation in the physiology
of individuals, particularly for generalist fish species that occupy a range of different habitats
with different prey communities (Jiang & Carbines, 2002; Thrush et al., 2002; Szedlmayer &
Lee, 2004).

Parapercis colias are an important commercial and recreational fishery species in New
Zealand, that occupy biogenic habitats located on the seafloor (Jiang & Carbines, 2002;
Carbines et al., 2004; MPI, 2021). Adult P. colias are generalist carnivores that feed on a
variety of crustaceans, molluscs, fish, polychaetes, and echinoderms, depending on what is
available in their local habitat (Jiang & Carbines, 2002; Carbines et al., 2004). P. colias diets
have also been observed to change as individuals increase in size in northern New Zealand,
with juveniles consuming more amphipods and isopods, and adults consuming more crabs

43
and ophiuroids (Mutch, 1983; Jiang & Carbines, 2002). However, no studies have explored the
diets of juveniles in biogenic habitats in the Marlborough Sounds.

In this chapter, I quantified the diet of juvenile P. colias from the Marlborough Sounds, New
Zealand and investigated differences in diet among habitats, to assess the quality and value
of juvenile P. colias nursery habitats. I used contents found in juvenile P. colias stomachs to
evaluate variation in the diet among 5 different nursery habitats (biogenic clumps, bryozoans,
dog cockles, horse mussels, and reef edges). Specifically, I addressed five questions: (1) Do
feeding opportunities differ among habitats? (2) Does the diversity of prey in the diet differ
among habitats? (3) Does the abundance of certain prey types in the diet differ among
habitats? (4) Does the biomass of certain prey types in the diet differ among habitats? (5)
Does the diet change as juveniles increase in size?

44
3.2. Methods

3.2.1. Extraction of prey items from stomachs

To test whether the diet of juvenile P. colias differed among potential nursery habitats,
juvenile P. colias guts were taken from the same fish used for otolith analyses (see Chapter 2
for details). Guts were processed from March 2021 to June 2021 at the Wellington University
Coastal Ecology Lab (WUCEL). The stomach of each sample was identified by locating the
pyloric caeca, which helped to distinguish between the stomach and intestine. Stomach
contents were extracted to a petri dish and then washed through a 119 µm sieve with 70%
ethanol to separate the contents. Stomach contents were then transferred into a Bogorov
counting chamber for further examination. Stomach contents were examined under a
dissecting microscope (Olympus SZ61) at 2X magnification. Each time a different prey species
appeared, a photo was taken of that species using a DSLR camera (Canon EOS 70D) attached
to the dissecting microscope set at 2X magnification. Each prey item was counted and
measured in length to the nearest division on the graticule scale, which was converted later
to mm.

3.2.2. Differences in feeding opportunities among habitats

To determine whether feeding opportunities differed among habitats, stomachs not
containing prey items were classified as empty, while stomachs containing prey items were
classified as full. Pearson’s chi-squared was conducted in R (version 4.0.3) at the 5%
significance level to compare the frequency of empty stomachs among habitats.

3.2.3. Differences in prey diversity among habitats

To determine whether the diversity of prey items differed among habitats, three different
measures of diversity were compared: species richness, Shannon’s diversity index, and
species evenness. Each prey item found was identified to the lowest taxonomic level possible
and allocated to 1 of 12 different taxonomic groups. For each fish, species richness was
measured as the number of different taxonomic groups. Shannon’s diversity index was
calculated by the equation: 𝐻" = − ∑$#%& 𝑝# ln 𝑝# , where H’ is the diversity index, s is the
number of species (taxa), and pi is the proportion of individuals belonging to the ith species
(taxa). Species evenness was calculated by the equation: 𝐽" = 𝐻" / log 𝑆, where J’ is species

45
evenness, H’ is Shannon’s diversity index, and S is the number of species (taxa). Higher values
indicate greater diversity. ANOVA was conducted in R (version 4.0.3) at the 5% significance
level to compare species richness, Shannon’s diversity index, and species evenness among
habitats.

3.2.4. Differences in prey abundance among habitats

To determine whether the number of prey items in each prey group differed among habitats,
the number of identifiable prey items in each prey group was recorded. For most crustacean
prey groups, items were only counted when at least the carapace was present. Amphipods
were only counted when most of the head and body were present, polychaetes were only
counted when at least the head or segments were present, gastropods were only counted
when any distinguishable body part was present, and fish were only counted when most of
the head and body were present. ANOVA was conducted in R (version 4.0.3) at the 5%
significance level to compare the abundance of prey items in each taxa among habitats.

3.2.5. Differences in prey biomass among habitats

To determine whether the biomass of prey items in each group differed among habitats, prey
biomass was estimated by using the sieve size classes and mean ash-free dry weight values
from Edgar (1990). Each prey item was allocated to 1 of 8 different sieve size classes (0.5,
0.71, 1.0, 1.4, 2.0, 2.8, 4.0, 5.6 mm). Each sieve size class contains prey that are equal to or
larger than the sieve size. For each prey group in each stomach, the biomass of invertebrate
prey was calculated by multiplying the number of that prey item by the mean ash-free dry
weight (AFDW) in each sieve size. Fish prey were allocated to the same sieve size classes, but
biomass was calculated by multiplying the number of fish by the weight, which was estimated
by using the fish length-weight relationship equation: 𝑊 = 𝑎𝐿! , where W is the expected
weight, a is a constant and scaling coefficient for the weight at length, L is the measured
length, and b is a parameter for body shape and the type of growth. Generic values of a = 0.01
and b = 3 (isometric growth) were used because fish could not be clearly identified (Le Cren,
1951). The biomass in each sieve size class was then added together to calculate the total
biomass of each prey group. ANOVA was conducted in R (version 4.0.3) at the 5% significance
level to compare the biomass of each taxa among habitats.

46
3.2.6. Changes in diet with increasing juvenile size
To determine whether the diet of juvenile P. colias changed when they increased in size, each
juvenile was allocated to a 5 mm size (length) class and ANOVA was used to compare prey
diversity among size classes in each habitat. Additionally, linear regression was used to
determine if there was a correlation between juvenile length and prey diversity (species
richness, Shannon’s diversity index, species evenness), and between juvenile length and the
abundance of each prey taxa group. All statistical analyses were conducted in R (version 4.0.3)
at the 5% significance level.

47
3.3. Results

3.3.1. Differences in feeding opportunities among habitats

Out of the 309 juvenile P. colias stomachs processed, 242 contained prey items, while 67 did
not. Biogenic clumps had the highest proportion of stomachs with prey items present (89.3%),
followed by horse mussels (87.0%), dog cockles (75.0%), reef edges (73.2%), and then
bryozoans (72.0%) (Figure 3.1). Pearson’s chi-squared test showed no significant difference
in the frequency of empty stomachs among habitats.

140

120
34
Number of stomachs

100

80
10
60 Empty
13 93 Full
40
67
3
20 7 39
25 18
0
Biogenic Bryozoans Dog Cockles Horse Mussels Reef Edge
Clumps
Habitat

Figure 3.1. Number of stomachs that were full or empty in each habitat. The total number of
stomachs in each habitat were: biogenic clumps (n = 28), bryozoans (n = 25), dog cockles (n =
52), horse mussels (n = 77), and reef edge (n = 127).

3.3.2. Differences in prey diversity among habitats

A total of 12 different prey taxa groups were identified in the stomachs of juvenile P. colias.
This included 8 crustacean groups (gammarids, mysids, true crabs, hermit crabs, cumaceans,
caprellids, true shrimps, squat lobsters), 2 mollusc groups (bivalves, gastropods), polychaetes,
and fish. Not all prey groups were found across all habitats. Caprellids were only found in
juveniles from reef edges, cumaceans and true shrimps were not found in juveniles from
bryozoans, bivalves were not found in juveniles from reef edges, squat lobsters and

48
gastropods were not found in juveniles from dog cockles, and gastropods were not found in
juveniles from biogenic clumps. Species richness was significantly higher in the diet of
juveniles from horse mussels than in those from bryozoans and reef edges (F4, 237 = 5.736, p <
0.001). Post hoc analyses (Tukey’s test) showed that juveniles from horse mussels had an
average 0.64 more prey items than juveniles from bryozoans, and 0.52 more than reef edges
(Figure 3.2).

2.2
b
Mean species richness of prey

2
ab
ab
1.8
a
1.6 a

1.4

1.2

1
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 3.2. Mean species richness (± SE) of prey found in juvenile P. colias stomachs from each
habitat. Lowercase letters denote groups with similar means.

Shannon’s diversity index was significantly higher in the diet of juveniles from horse mussels
than in those from reef edges (F4, 237 = 4.339, p = 0.002). Post hoc analyses (Tukey’s test)
showed that the index was an average 0.24 higher in juveniles from horse mussels than in
reef edges (Figure 3.3).

49
 0.6

Mean Shannon diversity index of prey

b
0.5 ab ab

0.4
a
ab
0.3

0.2

0.1

0
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 3.3. Mean Shannon diversity index (± SE) of prey found in juvenile P. colias stomachs
from each habitat. Lowercase letters denote groups with similar means.

Species evenness was significantly higher in the diet of juveniles from horse mussels than in
those from reef edges (F4, 237 = 3.224, p = 0.013). Post hoc analyses (Tukey’s test) showed that
this was an average 0.47 higher in juveniles from horse mussels than in reef edges (Figure
3.4).

50
 1.6
ab
Mean species evenness of prey 1.4 ab b

1.2

1 ab a

0.8

0.6

0.4

0.2

0
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 3.4. Mean species evenness (± SE) of prey found in juvenile P. colias stomachs from
each habitat. Lowercase letters denote groups with similar means.

3.3.3. Differences in prey abundance among habitats

Crustaceans were the most abundant prey item found, accounting for 79.4 to 98.7% of prey
items found in juvenile P. colias stomachs across all habitats. Polychaetes (0.9-8.8%), molluscs
(0.1-8.8%), and fish (0.3-2.9%) only made up a small portion of the diet across all habitats
(Figure 3.5). When separating crustaceans and molluscs into more specific taxonomic groups,
gammarids were the most abundant prey item in reef edge (82.3%), horse mussel (57.0%),
dog cockle (35.5%), and biogenic clump (62.3%) habitats, but mysids were the most dominant
prey item (50.0%) in bryozoan habitats (Figure 3.6).

51
 Reef Edge

Horse Mussels
Habitat

Crustaceans
Dog Cockles
Polychaetes
Molluscs
Bryozoans
Fish

Biogenic Clumps

0 10 20 30 40 50 60 70 80 90 100
Prey abundance proportion (%)

Figure 3.5. Proportion of prey taxa groups in each habitat.

Reef Edge Gammarids

Mysids
True Crabs
Horse Mussels
Hermit Crabs
Habitat

Polychaetes
Dog Cockles
Cumaceans
Caprellids
Bryozoans
True Shrimps
Bivalves
Biogenic Clumps Fish
Squat Lobsters
0 10 20 30 40 50 60 70 80 90 100
Gastropods
Prey abundance proportion (%)

Figure 3.6. Proportion of prey taxa groups in each habitat, with crustaceans and molluscs
separated into more specific taxa.

52
Prey abundance was significantly higher in the diet of juveniles from reef edges than those in
bryozoans and dog cockles (F4, 237 = 4.145, p = 0.003). Post hoc analyses (Tukey’s test) showed
there were an average of 5.3 more prey items in juveniles from reef edges than in bryozoans,
and 4.5 more than in dog cockles (Figure 3.7).

9
b
8

7
ab
Mean abundance

5 ab
a
4
a
3

0
Biogenic Clumps Bryozoans Dog Cockles Horse Mussels Reef Edge
Habitat

Figure 3.7. Mean abundance (± SE) of prey found in the stomachs of juvenile P. colias from
each habitat. Lowercase letters denote groups with similar means.

Crustaceans were significantly more abundant prey found in the stomachs of juvenile P. colias
from reef edges than in bryozoans and dog cockles (F4, 237 = 4.377, p = 0.002), while molluscs
were significantly more abundant prey in bryozoans than in reef edges (F4, 237 = 2.823, p =
0.026). Post hoc analyses (Tukey’s test) showed that there were an average 5.6 more
crustaceans in juveniles from reef edges than in bryozoans, and 4.6 more than in juveniles
from dog cockles. There were an average 0.16 more molluscs in juveniles from bryozoans than
in reef edges. When separating crustaceans and molluscs into more specific taxonomic
groups, gammarids were significantly more abundant prey found in the stomachs of juveniles
from reef edges than in bryozoans, dog cockles, and horse mussels (F4, 237 = 5.14, p < 0.001),
while cumaceans were more abundant in juveniles from horse mussels than in dog cockles
and reef edges (F4, 237 = 3.803, p = 0.005). Post hoc analyses showed that there were an

53
average 5.7 more gammarids in juveniles from reef edges than in bryozoans, 5.0 more than
in juveniles from dog cockles, and 3.2 more than in juveniles from horse mussels. There were
an average 0.17 more cumaceans in juveniles from horse mussels than in dog cockles, and
0.15 more than in juveniles from reef edges (Figure 3.8). No significant differences were found
for other prey groups.

54
 A B
9 b 0.30
b
8 ab 0.25
7
6 ab a 0.20
5 ab
a 0.15 ab
4 ab
3 0.10 a
2
0.05
1
0 0.00
Dog Cockles

Dog Cockles
Reef Edge

Reef Edge
Biogenic Clumps

Bryozoans

Horse Mussels

Biogenic Clumps

Bryozoans

Horse Mussels
Mean abundance

C D
8 0.30
b b
7 0.25
6
a 0.20
5 ab
ab
4 a 0.15 a
a
3 a 0.10 ab
2
1 0.05
0 0.00
Biogenic Clumps

Bryozoans

Dog Cockles

Horse Mussels

Biogenic Clumps

Bryozoans

Dog Cockles

Horse Mussels
Reef Edge

Reef Edge

Habitat

Figure 3.8. Prey taxa where mean abundance (± SE) was significantly different among
habitats: (A) crustaceans, (B) molluscs, (C) gammarids, and (D) cumaceans. Lowercase letters
denote groups with similar means.

3.3.4. Differences in prey biomass among habitats

Crustaceans made up the most prey biomass, accounting for 79.4% to 98.7% of the total prey
biomass in each habitat. Polychaetes (4.5-14.3%), molluscs (0.1-5.8%), and fish (0.3-0.9%)
only accounted for a small portion of the diet across all habitats (Figure 3.9). When separating

55
crustaceans and molluscs into more specific taxonomic groups, mysids made up the most prey
biomass in reef edge (36.8%), horse mussel (41.4%), dog cockle (50.0%), and bryozoan (62.1%)
habitats, while gammarid biomass was only dominant in biogenic clump (57.7%) habitats
(Figure 3.10).

Reef Edge

Horse Mussels
Habitat

Crustaceans
Dog Cockles
Polychaetes
Molluscs
Bryozoans
Fish

Biogenic Clumps

0 10 20 30 40 50 60 70 80 90 100
Prey biomass proportion (%)

Figure 3.9. Proportion of biomass for each prey taxa in each habitat.

56
 Reef Edge Gammarids
Mysids
Polychaetes
Horse Mussels
Hermit Crabs
Habitat

True Crabs
Dog Cockles
True Shrimps
Squat Lobsters
Bryozoans
Cumaceans
Bivalves
Biogenic Clumps Fish
Caprellids
0 10 20 30 40 50 60 70 80 90 100
Gastropods
Prey biomass proportion (%)

Figure 3.10. Proportion of biomass for each prey taxa in each habitat, with crustaceans and
molluscs separated into more specific taxa.

Overall mean prey biomass in the stomachs of juvenile P. colias was not significantly different
among habitats. Mollusc biomass was significantly higher in juveniles from bryozoans than in
reef edges (F4, 237 = 3.026, p = 0.019). Post hoc analyses (Tukey’s test) showed that average
mollusc biomass was 0.79 mg higher in juveniles from bryozoans than in reef edges. When
separating crustaceans and molluscs into more specific taxonomic groups, gammarid biomass
was significantly higher in juveniles from biogenic clumps than in all other habitats, and higher
in juveniles from reef edges than in bryozoans (F4, 237 = 8.14, p < 0.001). Cumacean biomass
was significantly higher in juveniles from horse mussels than in reef edges (F4, 237 = 2.592, p =
0.037). Gastropod biomass was significantly higher in juveniles from bryozoans than in all
other habitats (F4, 237 = 2.952, p = 0.021). Post hoc analyses (Tukey’s test) showed that average
gammarid biomass was 8.5 mg higher in juveniles from biogenic clumps than in bryozoans,
5.7 mg higher than in juveniles from dog cockles, 6.5 mg higher than in juveniles from horse
mussels, 4.3 mg higher than in juveniles from reef edges, and 4.1 mg higher in juveniles from
reef edges than in bryozoans. Cumacean biomass was 0.77 mg higher in juveniles from horse
mussels than in reef edges. Gastropod biomass was 0.37 mg higher in juveniles from
bryozoans than in horse mussels and reef edges, and 0.38 mg higher than in juveniles from

57
 biogenic clumps and dog cockles, both of which did not have any gastropods. Squat lobster
biomass was significantly different among habitats (F4, 237 = 2.45, p = 0.047) but post hoc
analyses did not show any significant pairwise differences, biomass appears to be higher in
juveniles from bryozoans than in all other habitats (Figure 3.11). No significant differences
were found for other prey groups.

A B
1.4 b 12
c
1.2 10
1.0 b
8
0.8 ab
ab 6 ab
0.6 ab
ab a 4 a
0.4
0.2 2
0.0 0
Biogenic Clumps

Bryozoans

Dog Cockles

Horse Mussels

Biogenic Clumps

Bryozoans

Dog Cockles

Horse Mussels
Reef Edge

Reef Edge
C D
3.0 a 1.4 b
2.5 1.2
1.0
Mean biomass (mg)

2.0 a
0.8 ab
1.5
a 0.6 a
1.0 a a ab ab
0.4
0.5 0.2
0.0 0.0
Biogenic Clumps

Dog Cockles

Biogenic Clumps

Dog Cockles
Reef Edge

Reef Edge
Bryozoans

Horse Mussels

Bryozoans

Horse Mussels

58
 E
1.0
b
0.8

0.6

0.4
a a a a
0.2

0.0

Dog Cockles

Reef Edge
Biogenic Clumps

Bryozoans

Horse Mussels
Habitat

Figure 3.11. Prey taxa where mean biomass (± SE) was significantly different among habitats:
(A) molluscs, (B) gammarids, (C) squat lobsters, (D) cumaceans, and (E) gastropods. Lowercase
letters denote groups with similar means.

3.3.5. Changes in diet with increasing juvenile size

More prey taxa groups were found in the stomachs of larger juvenile P. colias size classes in
all habitats. However, one prey taxa group was always dominant in all size classes across all
habitats. Crustaceans were the most dominant type of prey item found in all juvenile P. colias
size classes across all habitats except for the 105-109 mm size class in dog cockles, where
bivalves were dominant in one sample. For juvenile P. colias from biogenic clumps, gammarids
were the most dominant prey item found in all but the 70-74 mm size class where mysids
were dominant. For juveniles from bryozoans, gammarids were the most dominant prey item
found in the 50-54 and 85-89 mm size classes, and mysids were the most dominant prey item
found in the 70-74, 80-84, and 90-94 mm size classes. For juveniles from dog cockles,
gammarids were the most dominant prey item found in the 60-64, 65-90, 75-79, 95-99 mm
size classes, mysids were the most dominant prey item found in the 80-84, and 85-89 mm size
classes, true crabs were the most dominant prey item found in the 90-94 mm size class, and
bivalves were the most dominant prey item found in the 105-109 mm size class. For juveniles
from horse mussels, gammarids were the most dominant prey item found in all but the 100-

59
 Proportion (%)

100
100

10
20
30
40
50
60
70
80
90
10
20
30
40
50
60
70
80
90

0
0
45-49 (0) 45-49 (0)
50-54 (0) 50-54 (1)
55-59 (0) 55-59 (2)
60-64 (1) 60-64 (0)
65-69 (2) 65-69 (0)
70-74 (0) 70-74 (2)

C
A
75-79 (3) 75-79 (7)
80-84 (10) 80-84 (5)
85-89 (10) 85-89 (3)
90-94 (7) 90-94 (5)
95-99 (5) 95-99 (0)
100-104 (0) 100-104 (0)
105-109 (1) 105-109 (0)
where mysids were dominant (Figure 3.12).

100
100

10
20
30
40
50
60
70
80
90
10
20
30
40
50
60
70
80
90

0
0
45-49 (1) 45-49 (0)
50-54 (0) 50-54 (1)
55-59 (0) 55-59 (0)
60-64 (0) 60-64 (0)
65-69 (0) 65-69 (0)
70-74 (4) 70-74 (1)
B

D
75-79 (4) 75-79 (0)
80-84 (12) 80-84 (6)
85-89 (23) 85-89 (5)
90-94 (14) 90-94 (4)
95-99 (7) 95-99 (1)
100-104 (2) 100-104 (0)
105-109 (0) 105-109 (0)
were the most dominant prey item found in all but the 70-74 and 100-104 mm size classes
104 mm size class where mysids were dominant. For juveniles from reef edges, gammarids

60
 E
100
90
80
70
60
50
40
30
20
10
0
85-89 (15)
90-94 (15)
95-99 (24)
100-104 (8)
105-109 (5)
45-49 (3)
50-54 (3)
55-59 (5)
60-64 (3)
65-69 (4)
70-74 (1)
75-79 (0)
80-84 (7)

Juvenile size class (mm)

Figure 3.12. Proportions of prey taxa in each juvenile size class for each habitat: (A) biogenic
clumps, (B) bryozoans, (C) dog cockles, (D) horse mussels, and (E) reef edges. Numbers in
parentheses denote the number of stomachs.

No significant differences in any of the three diversity measures were found among juvenile
size classes in any of the habitats. Furthermore, no significant relationships were found
between juvenile length and any of the three prey diversity measures in any of the habitats.
Gammarid abundance significantly decreased with increased juvenile length in dog cockles
(R2 = 0.13, F1, 37 = 5.43, p = 0.025), and mysid abundance significantly decreased with increased
juvenile length in reef edges (R2 = 0.04758, F1, 91 = 4.546, p = 0.036) (Figure 3.13).

61
 A B
60 30

50 25
Proportion (%)

40 20

30 15

20 10

10 5

0 0
40 60 80 100 40 60 80 100

Juvenile length (mm)

Figure 3.13. Abundance versus length for prey taxa groups where at least one significant
relationship was present: (A) gammarids in the stomachs of juveniles from dog cockles
(Abundance = 6.37 + -0.063*Length), and (B) mysids in the stomachs of juveniles from reef
edges (Abundance = 2.18 + -0.018*Length).

62
3.4. Discussion

Juvenile P. colias showed significant differences in stomach contents among habitats,

demonstrating the importance of habitat type in providing food, and reinforcing the
importance of habitat type on juvenile growth, examined in Chapter 2. Comparisons of the
frequency and proportion of empty stomachs among habitats showed no significant
differences, suggesting that feeding opportunities are the same across juvenile P. colias
nurseries.

Comparisons of the diversity of prey found in juvenile P. colias stomachs among habitats
showed that juveniles from horse mussels had significantly more diverse prey than juveniles
from reef edges when comparing species richness, Shannon’s diversity index, and species
evenness. Additionally, juveniles from horse mussels also had significantly more diverse prey
than juveniles from bryozoans when comparing species richness.

Overall, comparisons of the abundance and proportion of different prey taxa groups found in
juvenile P. colias stomachs among habitats showed that crustaceans were the most dominant
prey type in juveniles from all habitats. In particular, gammarids, a type of amphipod, were
the most dominant prey type in all but juveniles from bryozoans, where mysids were
dominant. When comparing the mean abundance of prey among habitats, juveniles from reef
edges had significantly more prey than juveniles from bryozoans and dog cockles.
Additionally, comparisons showed differences in the abundance of crustaceans, molluscs,
gammarids, and cumaceans among habitats.

Overall, comparisons of the biomass and proportion of different prey taxa groups found in
juvenile P. colias stomachs among habitats showed that crustaceans made up the most prey
biomass in juveniles from all habitats. In particular, mysids were the most dominant prey type
in all but juveniles from biogenic clumps, where gammarids were dominant. When comparing
the mean biomass of prey among habitats, no significant difference was found. However,
comparisons showed differences in the biomass of molluscs, gammarids, squat lobsters,
cumaceans, and gastropods among habitats.

63
Overall, comparisons of the abundance and proportion of different prey taxa groups among
5 mm juvenile size classes in each habitat showed that crustaceans were the most dominant
prey type in almost all size classes across all habitats, and were primarily gammarids and
mysids. Additionally, more prey types were often found in the stomachs of larger juveniles in
all habitats. However, when comparing the mean diversity of prey among size classes in each
habitat, no significant differences were found. No significant relationships between juvenile
length and prey diversity were found either. Although, gammarid abundance decreased with
increasing juvenile length in dog cockles, and mysid abundance decreased with increasing
juvenile length in reef edges.

My results suggest that feeding opportunities or the ability for juveniles to capture prey do
not differ among habitats, similar to a previous study by Jiang and Carbines (2002). However,
P. colias are known to regurgitate their food, which empties the entire stomach of natural
prey and makes it difficult to discern whether the presence of empty stomachs is due to the
ability to capture prey or a result of regurgitation (Jiang & Carbines, 2002). In either case, my
results suggest that the ability to capture prey or the rate of regurgitation is the same among
habitats. The stomachs of juveniles from reef edge habitats had significantly more prey on
average than other habitats, suggesting that the availability of food is greater in reef edges.
However, the overall biomass of prey found in juvenile stomachs did not differ among
habitats. Although prey might be more abundant in reef edges, this suggests that prey found
in these habitats might be comparatively smaller in size than other habitats. Juveniles from
reef edges might need to capture more individual prey items to make up for smaller prey
sizes. This would need to be further tested by comparing the sizes of prey among habitats,
rather than just the biomass. The greater diversity of prey found in the stomachs of juveniles
from horse mussels are indicative of the habitat’s ability to support more diverse prey
communities and a more diverse diet for juveniles (McLeod et al., 2014). The dominance of
gammarids in both abundance and biomass in the diets of most juveniles is similar to a
previous study by Mutch (1983) that observed juvenile P. colias in northern New Zealand
consuming more amphipods. This suggests that amphipods, particularly gammarids, are an
important and valuable prey item in juvenile P. colias diets. Furthermore, the dominance of
crustaceans and the presence of various molluscs, fish, and polychaetes, depending on what
is available in the local habitat, is consistent with previous studies on adults (Mutch, 1983;

64
Jiang & Carbines, 2002; Carbines et al., 2004). Additionally, the crustacean-dominated diets
seen in juvenile P. colias are consistent with other juvenile fish species, highlighting the
importance of crustaceans in juvenile fish diets (Lowe, 2012; Usmar, 2012). Although
gammarids were dominant in most size classes, the presence of more different prey taxa, and
decrease in gammarid abundance (only seen in dog cockles) with increasing juvenile size is
also similar to Mutch (1983), who observed a shift from amphipods and isopods in juveniles,
to crabs and ophiuroids in adults, for P. colias in northern New Zealand.

This research highlighted the importance of habitat type in mediating the diet of juvenile P.
colias suggesting that the quality and availability of food varies among different nursery
habitats. Knowledge of the diets of juveniles living in different habitats are important in
furthering our understanding of what drives differences in predator-prey interactions,
foraging strategies, and growth among different nursery habitats.

65
 Chapter 4: Conclusions

4.1. Summary of findings

Knowledge of the qualities and factors that make nursery habitats valuable are critical to our
understanding of what drives the success of fish populations. This thesis highlighted the
importance of nursery habitat type in driving the success of juvenile P. colias populations.
Juvenile P. colias showed stark differences in growth and diet among different nursery
habitats, suggesting that different habitat types vary in quality and not all nurseries are equal
in value. In Chapter 2, comparisons of growth showed that juvenile P. colias collected from
reef edge habitats were typically larger, heavier, in better body condition, and had
significantly faster growth compared to juveniles from other habitats, particularly when
compared with juveniles from bryozoan habitats. In Chapter 3, comparisons of juvenile P.
colias diets among habitats showed that food availability may be higher in reef edge habitats,
with juveniles possessing significantly more prey items than other habitats. Crustaceans,
particularly gammarids and mysids, were the most dominant prey found in the stomachs of
juveniles from all habitats in both abundance and biomass. Juvenile diets also showed clear
differences in prey diversity, as well as the abundance and biomass of certain prey taxa among
habitats. Furthermore, changes in the diet were observed with increasing juvenile size.

4.2. Limitations
Quantifying the growth of live juvenile fish can be challenging in the marine environment
because juveniles are often quite difficult to capture and handle, which is why growth studies
and fisheries scientists tend to estimate growth from lengths, weights, ages, and otolith
growth increments (Kimura, 1980; Chen et al., 1992; Vigliola & Meekhan, 2009; Walsh, 2017).
The accuracy of aging fish in this research could have been improved using a more precise
method of polishing otoliths that makes daily growth increments more visible across the full
counting axis, and could increase the success rate of otoliths appropriate for aging (Karakiri &
von Westernhagen, 1988). Multiple reads of each otolith, with increments approved by two
experienced readers, could also improve the accuracy of aging (Walsh, 2017). When binning
juvenile P. colias lengths into 5 mm size classes to test for changes in diet with increasing
juvenile size, sample sizes could have been larger in some size classes to better represent the

66
diet in those size classes. This was particularly the case for juveniles in the 105-109 mm size
class from dog cockles, which only had one sample, and was the only size class in this habitat
to have a bivalve-dominated diet.

4.3. Future directions

Analyses of juvenile P. colias diets among habitats in Chapter 3 revealed information that
could be linked to analyses of juvenile P. colias growth among habitats in Chapter 2. In
particular, juveniles from reef edges showed significantly faster growth with higher
abundances of prey items, crustaceans, and gammarids, while juveniles from bryozoans
showed significantly slower growth with lower abundances of prey items and gammarids.
These observations suggest that food availability, particularly the availability of gammarids, is
a driver of the differences in juvenile P. colias growth among habitats. It is possible that
gammarids provide some sort of nutritional benefit to growth, although this would need to
be further tested by analysing and comparing the contents of nutrients such as
carbohydrates, proteins, lipids, vitamins, and minerals (Shreck & Moyle, 1990). Although the
proportions of prey taxa found in the stomachs of juvenile P. colias can be indicative of the
structure of prey communities in each habitat, a more thorough approach is required to fully
represent the assemblages of prey in each habitat. The collection of habitat samples by
methods such as sediment cores or enclosing bags are critical for evaluating the full structure
of prey communities in biogenic habitats (Heck & Orth, 1980; Lowe, 2012). Furthermore, prey
assemblages determined by habitat samples could be compared with diets to provide
stronger evidence for prey selectivity and feeding strategies (Vanderpham et al., 2013;
Hempson et al., 2017).

4.4. Management implications

Anthropogenic activities have significantly impacted the marine environment and are well
known to have adverse effects on biogenic habitats, particularly those occurring in coastal
waters (Jackson et al., 2001). The epifaunal and infaunal communities living on the surface
and inside biogenic habitats are an important food source for many fish species, and are well
known to be affected by harmful activities such as bottom trawling (Hiddink et al., 2019),
shellfish dredging (Cranfield et al., 2004), sedimentation (Cunning et al., 2019) and the
deposition of toxic chemicals (Roberts et al., 2008). Dead biogenic habitats are well known to

67
show significant losses of epifaunal and infaunal communities, reducing the diversity,
production, and abundance of available prey (Sheehan et al., 2015; Gabara et al., 2018).
Although the Marlborough Sounds in New Zealand has been a popular fishing ground for P.
colias, continuous bottom trawling, scallop dredging, and coastal development will likely
cause P. colias habitats to become much less widespread in the future, and amplify population
bottlenecks (Carbines et al., 2004; Morrison et al., 2009). Similar scenarios could be seen for
other fishery species in New Zealand (Morrison et al., 2009), such as Chrysophrys auratus (also
known as Pagrus auratus or Australasian snapper). Found mostly in the North Island, C.
auratus rely on seagrass beds as nurseries for rearing juveniles (Lowe, 2012; Parsons et al.,
2016). Seagrass beds in northern New Zealand have also been damaged by anthropogenic
activities, affecting the growth and condition of juvenile populations (Turner & Schwarz, 2006;
Stewart, 2018). Furthermore, similar scenarios could also be seen for other fish species
around the world, particularly in tropical regions, where coral reefs support a diverse array of
fisheries species but are under immense pressure from coastal development and climate
change (Hughes et al., 2003; Munday et al., 2008; Hoegh-Guldberg, 2011; Rogers et al., 2014).
Knowledge of the qualities that make nursery habitats valuable to fisheries species is critical
to understanding how fish stocks respond to human impacts, and predicting how fish stocks
might change in the future. My thesis provides important information for the modelling and
management of P. colias stocks in New Zealand, and takes one of the first essential steps
towards the goals of the ‘Juvenile fish habitat bottlenecks’ programme. The ‘Juvenile fish
habitat bottlenecks’ programme aims to identify and alleviate juvenile habitat bottlenecks for
three coastal fisheries species (Parapercis colias/blue cod, Chrysophrys auratus/Australasian
snapper, and Nemadactylus macropterus/tarakihi) in New Zealand. A combination of
regional-scale surveys, and observational and experimental studies will provide empirical
data that can be used in simulation models for evaluating fisheries management. These
models can predict how different scenarios will affect fish stocks, and contribute to the
development of the best management strategies for productive and sustainable fisheries in
New Zealand.

68
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