Mate Choice, Parental Care and Foraging

Behaviour of the northern trout gudgeon

Mogurnda mogurnda (Pisces: Eleotridae)

A thesis submitted for the degree of Master of Philosophy

at the Australian National University

Michelle A. Shackleton

March 2007

DECLARATION

I declare that this thesis is all my own work and that all sources used have been

acknowledged.

M A Shackleton

ACKNOWLEDGEMENTS

I would like to thank my supervisor Michael Jennions for all his help over the many

years he has had the dubious honour of being my supervisor, as well as Alan Muir and the

other support staff for their help with all my numerous logistical issues. Thanks also to my

supervisory panel members Pat Backwell, Scott Keogh and Rob Magrath. A special thank

you to Bob Wong for showing me the ropes and always being so generous with his time and

invaluable advice. I’d also like to thank Dave Wilson for providing me with the gudgeons from

up in Darwin, and David Linterman for his patience and support with the two-spined

blackfish.

A very special thanks to Leeann Reaney without whom I would never have managed

to finish this, and for whose friendship I am eternally grateful. Thanks also to Golo Maurer for

doing it first so I could see what I was in for, and for always somehow finding the time to be

there if I needed him. Thanks to my other colleagues and friends Rachel Sims, Stuart

Cooney, Jean Drayton and Erika Alacs for their support both in and out of university. And

special appreciation too goes to my personal motivator Heather, who always knows the right

thing to say.

The biggest thank you of all goes to my parents for educating me in all aspects of life:

they have never wavered in their total support of everything I’ve done, and have always been

there when I needed them: this is for you.

TABLE OF CONTENTS

ABSTRACT.............................................................................................................................................1

CHAPTER 1 GENERAL INTRODUCTION................................................................ 31.1 Sexual selection.........................................................................................................................3

1.1.1. An overview............................................................................................................................3

1.2 Female choice and male competition...................................................................................... 4

1.3 Direct benefits model................................................................................................................ 6

1.4 Indirect benefits of female choice............................................................................................ 6

1.4.1. Genetic compatability.............................................................................................................7

1.4.2. “Good genes” model.............................................................................................................. 7

1.4.3. The Fisher process................................................................................................................ 7

1.4.4. The Lek paradox.................................................................................................................... 8

1.4.5. Strength of indirect selection................................................................................................. 9

1.5 Sexual conflict...........................................................................................................................9

1.6 Male-male dominance............................................................................................................111.7 Fish as models for parental care............................................................................................ 12

1.8 Parental care behaviours.........................................................................................................131.9 Variation in parental care.......................................................................................................151.10 Costs and benefits of parental care......................................................................................151.11 Honest Signalling...................................................................................................................161.12 Foraging: maximising energy gain.......................................................................................18

1.13 Aims of this study...................................................................................................................201.14 Study species..........................................................................................................................21References............................................................................................................................................24

CHAPTER 2 MATE CHOICE IN THE NORTHERN TROUT GUDGEON (MOGURNDA MOGURNDA).....................................................................................472.1 Introduction.............................................................................................................................47

2.1.1. Female mating preferences.................................................................................................. 47

2.1.2. Life history traits and female mating preferences................................................................47

2.1.3. Male dominance and female mating preferences................................................................48

2.1.4. Parental Care and Female Mating Preferences...................................................................50

2.1.5. Measuring female mating preference...................................................................................50

2.1.6. Aims of this study.................................................................................................................52

2.2 Methods...................................................................................................................................53

2.2.1. Pilot studies on male dominance.......................................................................................... 53

2.2.2. Mate choice trials..................................................................................................................54

2.2.3. Preference Criteria...............................................................................................................55

2.2.4. Statistical Analyses - Mate Choice Analysis........................................................................ 56

2.3 Results.....................................................................................................................................582.4 Discussion...............................................................................................................................71

2.4.1. Females preferred larger males........................................................................................... 71

2.4.2. Size assortative mating........................................................................................................72

2.4.3. Condition-dependent female choice.....................................................................................72

2.4.4. Comparing measures of mating preference.........................................................................74

References............................................................................................................................................75

CHAPTER 3 SPAWNING AND PARENTAL CARE IN THE NORTHERN TROUT GUDGEON (MOGURNDA MOGURNDA) ................................................................. 883.1 Introduction............................................................................................................................. 88

3.1.1. How much to invest in parental care: balancing costs and benefits....................................88

3.1.2. Paternal care in fish...............................................................................................................89

3.1.3. Sexual conflict over parental care.........................................................................................90

3.1.4. Adjusting parental investment: responding to partner effort................................................ 91

3.1.5. Adjusting parental investment: responding to partner condition..........................................92

3.1.6. Parental care and mate choice..............................................................................................93

3.1.7. Variation in parental care behaviours....................................................................................95

3.1.8. Aims of this study................................................................................................................. 97

3.2 Methods................................................................................................................................... 98

3.2.1. Parental Care........................................................................................................................98

3.2.2. Statistical Analyses - Parental Care Analysis...................................................................... 98

3.3 Results................................................................................................................................... 1003.4 Discussion............................................................................................................................. 108

3.4.1. Variation in parental care quality......................................................................................... 108

3.4.2. Variation in mate choice..................................................................................................... 110

References.......................................................................................................................................... 113

CHAPTER 4 FORAGING BEHAVIOUR AND SUBSTRATE DISCRIMINATION IN THE NORTHERN TROUT GUDGEON (MOGURNDA MOGURNDA)................... 1244.1 Introduction........................................................................................................................... 124

4.1.1 Food density and distribution............................................................................................. 124

4.1.2 Food density and Individual variation.................................................................................. 126

4.1.3 Microhabitat complexity...................................................................................................... 127

4.1.4 Discriminating between microhabitats................................................................................ 128

4.1.5 Aims of this study............................................................................................................... 130

4.2 Methods................................................................................................................................. 131

4.2.1 Binary Substrate Choice..................................................................................................... 131

4.2.2 Statistical Analyses - Foraging Analysis............................................................................ 132

4.3 Results................................................................................................................................... 134

4.4 Discussion............................................................................................................................. 145

References.......................................................................................................................................... 148

CHAPTER 5 GENERAL DISCUSSION...............................................................1745.1 Aims of this study................................................................................................................. 174

5.2 Condition-dependent female choice................................................................................... 175

5.3 Parental care behaviours in M. Mogurnda......................................................................... 176

5.4 Maintaining a maladaptive preference............................................................................... 177

5.5 Comparing female choice tests........................................................................................... 178

5.6 Variation in expression of mating preference................................................................... 178

5.7 Cues to mating preference.................................................................................................. 179

5.8 Foraging................................................................................................................................. 180

5.9 Conclusion............................................................................................................................ 181

References......................................................................................................................................... 182

ABSTRACT

The parental role males play ranges from no male parental care to extensive male-only care.

Females may acquire either direct or indirect fitness benefits from mate choice. Direct fitness gains

include access to male parental care, and researchers have traditionally emphasized this benefit in

species with extensive male parental care. Larger, more dominant males are assumed to be better

mates that provide higher quality parental care but many new studies dispute these assumptions. The

assumption that females prefer dominant males is questionable because few studies fully control for

male-male competition. Also, higher parental quality is not always correlated with male size, although

evidence for other honest signals of parental quality is growing. Moreover, the accuracy of traditional

simultaneous choice tests is now disputed because recent studies show that when the results of such

association preference tests are compared to latency to mating tests, preferred characteristics are

often no longer preferred or different characteristics become indicators of male attractiveness.

Here I test how male size, female choice, and the quality of male parental care interact in the

northern trout gudgeon Mogurnda mogurnda. I aimed to identify any traits that present an honest

signal of male parental quality, and whether females were choosing males based on these

characteristics. I found that female M. mogurnda prefer larger males in simultaneous choice tests, and

some evidence for size-assortative mating as larger females tended to spend proportionally more time

with larger males. Larger females also exhibited a stronger preference for generally preferred males

than smaller females, implying that choice is condition-dependent. Comparing mate choice tests,

however, I found that male traits that were preferred in traditional association tests were not preferred

in latency tests. Instead, females took longer to spawn with preferred males, which directly

contradicted the results based on association time.

There was no correlation between male size and parental care. The only trait that correlated

with male care was male attractiveness (based on association tests). In the latency to mating tests, it

is unclear what traits females based their preference response on, but they spawned sooner with non­

preferred males (from association tests) who showed higher quality parental care (higher fanning rate)

than preferred males. Females could therefore still be choosing males based on an unmeasured trait

correlated with quality of care.

Foraging efficiency has an important effect on body size and condition so it is closely

associated with sexual selection as mate choice and parental are energetically expensive activities.

Recent work shows that some fish preferentially foraging around complex habitats, presumably due to

greater potential prey density, although other factors also influence foraging behaviour. I found that in

1 .

M. mogurnda there was no preference for “complex” over “simple” substrates. I conclude that the

greater potential for food created by the higher incidence of interstitial spaces indicates that increased

search and handling time associated with complex microhabitats and the lower energetic award from

smaller prey items may have balanced the preference between substrates.

CHAPTER 1 General Introduction

1.1 S e xu a l se lec tio n

1.1.1. An overview

The nature of sexual reproduction has lead to conflict between mates as they each try to

maximise their own lifetime reproductive output in the face of competition with members of the same

sex, and differences in interest between the sexes. Competition is inherent in the mechanism of

reproduction by anisogamy (the differentiation of the sexes by the size of their gametes) as many

small male gametes compete for a limited number of larger female gametes. Conflict is also present in

any situation where individuals who manipulate their mates stand to significantly increase their own

lifetime reproductive success by so doing, even if this results in a reduction in their mate’s lifetime

fitness.

Sexual selection occurs when members of each sex maximise their reproductive success in

different ways. Males produce much smaller and more numerous gametes than females and maximise

their reproductive output by mating with more females; mating with females that have greater

reproductive potential; and attaining a greater proportion of fertilisation for each reproductive event.

Females produce fewer and much larger gametes and maximise their reproductive success by mating

at an intermediate optimal rate and selecting the best “quality” males as their mates and, ultimately, as

the fertilisers of their eggs. This conflict between the sexes (and between individuals of the same sex)

leads to sexual selection.

Anisogamy results in many more male gametes (sperm) competing for far fewer female

gametes (eggs) and this creates competition between males. Males maximise their reproductive

success by maximising their number of mates, and by investing less into their current mating event

increase their future reproductive output. Successful males (i.e. those that females choose as mates

or that consistently out-compete other males) therefore tend to have a higher potential reproductive

rate (PRR) than the average female. As a result, these males are therefore inclined to invest less into

each reproductive event, so that females often have to compensate by investing more (Fisher 1930).

Females initially invest more than males into each offspring, as the production of eggs is

relatively more costly than producing sperm. This cost is small, however, in comparison to the costs of

parental care. Traditionally, females provide parental care while males invest more into finding mates.

The resulting male-biased operational sex ratio (OSR) exacerbates competition between males, and

3 .

completes a positive feedback loop by reducing competition between females for mates. This allows

females to invest more into parental care and, importantly, facilitates females being choosier. As

females become choosier, the pool of males that are likely to mates becomes smaller, so the PPR of

these males becomes even higher than that of females. This makes it even more worthwhile for these

males to invest less in care and more into seeking extra matings.

This, however, is not the whole story. Every offspring has one male and one female parent

(Fisher 1930) and therefore, given an equal adult sex ratio, overall males do not participate in more

matings than females. Thus greater competition between males due to a male-biased OSR does not

explain why males do not generally invest more into parental care (Kokko and Jennions 2003). Queller

(1997) shed some light on the situation, and suggested that multiple matings and sperm competition

leads to uncertainty in paternity and decreased benefits of investing in parental care for a male

compared to a female. For example, Neff (2003) showed experimentally that male bluegill sunfish

Lepomis macrochirus adjusted their parental effort in accordance with the perceived paternity of the

eggs in their nest, favouring clutches that they identified as being more closely related to them. Queller

(1997) also suggested that if a small proportion of males selected for by sexual selection enjoy higher

mating success, they have a higher breeding rate than the average male or the average female and

the costs of investing in parental care rather than seeking additionally mating opportunities are higher

for such males.

Fish have significantly contributed to research on mate choice behaviour. For example, three

spined sticklebacks Gasterosteus aculeatus have been used in ground-breaking research relating to

functions of visual signals (Tinbergen 1951) and were, in fact, the first species used to perform mate

choice experiments by artificially enhancing male secondary sexual characteristics (Semler 1971).

Studies on guppies Poecilia reticulata have been both prolific and innovative, including Endler’s

demonstration that predation selects for less colourful males even though females prefer more

colourful males (Endler 1980; 1983; 1988). Fish are also an excellent taxa for studying parental care

as they show all care systems (no care, biparental care, maternal care and paternal care) and care

behaviours in many forms, such as preparing nests [male common gobies, Pomatoschistus micropa

(Nyman 1953)] and caring for eggs [e.g., mouth brooding (Oppenheimer 1970)].

1.2 Female choice and male competition

Classical sex roles are that males compete, and females care and choose. This is not always

the case, however, and can even change during a breeding season (Lengkeek and Didderen 2006;

Shibata and Kohda 2006; Silva et al. 2006). To predict which sex will choose and which will compete

4 .

requires models that consider not only the OSR and PRR as models prior to Queller (1997) did (e.g.,

Clutton-Brock and Parker 1992; Parker and Simmons 1996), but also include variance in mate quality

(Johnstone et al. 1996) and, most importantly, the relatively new inclusion of life-history traits such as

the cost of breeding.

Mating is costly (Daly 1978; Pomiankowski 1988; Iwasa et al. 1991). Costs from mating

include an increased risk of predation (Sakaluk and Belwood 1984; Magnhagen 1991), and time and

energy costs from searching for males (e.g., Alatalo et al. 1988; Gibson and Bachman 1992).

Furthermore, mate choice increases these costs, which include energy spent to search for an

“acceptable” individual or fend off undesirable mates, lost mating opportunities from being selective, or

predation from increased searching behaviour (reviewed by Jennions and Petrie 1997). For example,

mate choice involves, by necessity, mate rejection, and male harassment and rejection of courting

males has shown to be is costly to female Drosophila melanogaster (Partridge and Fowler 1990;

Holland and Rice 1999). Godin and Briggs (1996) showed that female Trinidadian guppies Poecilia

reticulata reduced both their preference for bright males and their overall level of sexual activity when

the risk of predation was increased by the presence of a pike cichlid at a high predation site.

Interestingly, mate preference should be differentially costly with respect to female quality (Cotton et

al. 2006). Low quality females should suffer higher costs of mate preference than higher quality

females making the same mating decision, or higher quality females may be able to be more

discerning than poorer quality females for the same cost.

The question of how female mating preferences initially evolved and is maintained is still a key

question in the sexual selection literature. In a recent review, Kokko et al. (2006) outlined and detailed

various models of the evolution of sexual selection which I will discuss below. There is assumedly

something to be gained from the expression of mating biases or else it would be more beneficial to

mate randomly. If females choose males that provide increased benefits, selection will favour the

persistence of a female preference for the most beneficial males. This, in turn, will favour males that

provide these benefits, so the net result may be mutualistic coevolution driven by benefits (Eberhard

and Cordero 1995). Material reproductive gains that increase female lifespan reproductive success

are the most obvious, but not the only, benefits obtained from female choice. In addition, indirect

genetic benefits can lead to choosy females producing more viable and/or attractive offspring and

ultimately the production of relatively more grandchildren due to the greater reproductive success of

sexy sons (reviewed in Kokko et al. 2003).

5 .

1.3 Direct benefits model

Preference for direct benefits is favoured by natural selection because the preference itself

confers an increase in direct female fitness (Heywood 1989; Hoelzer 1989). For example, female

choice leading to direct material gains, such as nutritional gifts in spermatophores (e.g., Simmons and

Parker 1989), is under positive direct selection as it will increase female lifetime egg production and

imposes directional selection on males to signal this benefit (Price et al. 1993; Andersson 1994;

Kirkpatrick 1996). Male offerings can also include parental care, and exclusive paternal care may have

evolved in arthropods (Tallamy 2000) and territorial fish (Ah-King et al. 2005) because females prefer

males that provide parental care and paternal care was under direct selection. In extreme cases, male

investment in reproduction may exceed that of females [e.g., crickets (Simmons 1992)] and lead to

sex role reversal and male mate choice (e.g., Berglund and Rosenqvist 2003; LeBas et al. 2003). An

increase in female reproductive output offers the most straightforward explanation as to how mate

choice benefits can outweigh any costs of choice (Iwasa and Pomiankowski 1999), which explains

why it has been the main focus of research in many studies (e.g., Pizzari and Snook 2003; Wagner

and Harper 2003).

Alternately, the “sensory drive” or “sensory bias” model (West-Eberhard 1984; Ryan and Rand

1990; Endler and Basolo 1998; reviewed in Fuller et al. 2005) assumes that natural selection operates

directly on pre-existing sensory biases in circumstances other than mate choice, and may be the

initiating factor in the evolution of female choice (Kokko et al. 2003). For example, male guppies

Poecilia reticulata with greater orange colouration are more attractive to females possibly due to a

sensory bias toward orange food objects (Rodd et al. 2002). Female guppies, however, also use these

orange spots as indicators of male foraging ability and health (Endler 1980) as colour saturation is

condition-dependent (Houde and Torio 1992; Grether 2000; Kodric-Brown and Nicoletto 2005). So,

even when female choice has evolved from exploitation of a pre-existing sensory bias, direct or

indirect selection on the female preference may occur due to benefits accruing from better-quality

mates.

1.4 Indirect benefits of female choice

Situations where there appear to be no direct material benefits to mate choice are of particular

interest as they imply that there are compensatory indirect benefits to being choosy. Indirect benefits

arise due to the increased viability and/or the reproductive success of offspring, which subsequently

results in a greater number of descendents (Kokko et al. 2003).

6.

1.4.1. Genetic compatability

Choosy females can increase their fitness by reproducing with males that are more genetically

complimentary or compatible (e.g., Zeh and Zeh 1996; Brown 1997; 1997; Tregenza and Wedell

2000) due to such effects as increasing major histocompatibility complex heterozygosity (e.g., Landry

et al. 2001; Hoffman et al. 2007), inbreeding avoidance (e.g., Tregenza and Wedell 2002) and greater

offspring genetic diversity (Garant et al. 2005). For example, female fur seals go a greater distance in

a colony to conceive with males with lower relatedness, creating offspring with high heterozygosity

(Hoffman et al. 2007). Female choice for males on the basis of their genetic compatibility is, however,

not based on a linear directional preference for a male phenotypic trait (e.g., longer tails) and is

therefore difficult to observe.

1.4.2. “Good genes” model

Female choice can evolve rapidly if females show a preference for traits that are genetically

correlated with any trait favoured by direct selection such as male attractiveness or fecundity (and

ultimately with fitness) (Kokko et al. 2003). For example, females would receive indirect benefits of

female choice if they preferred males that are more colourful, and colourful males sire offspring that

have increased attractiveness or survival. Costly female mate choice might have originated and been

maintained by indirect genetic viability benefits to offspring provided by males (‘good genes’ model)

(e.g., Zahavi 1977; Andersson 1986; Pomiankowski 1987; Kirkpatrick and Ryan 1991; Moore 1994;

Kirkpatrick and Barton 1997). In support of this, female cockroaches Nauphoeta cinerea who mate

with attractive males produce offspring that hatch faster and reach sexual maturity sooner (Moore

1994). For numerous other cases of females mated to attractive males producing offspring with

increased viability, see Möller and Alatalo (1999). The good genes model predicts that female choice

imposes directional selection on males and the preference is under indirect positive selection through

the viability advantage conferred to the young.

1.4.3. The Fisher process

Instead of female choice being driven by the indirect benefits to offspring from inheriting

increased viability from the preferred male, its evolution may be driven by the simple fact that offspring

inherit the preference itself. Male offspring may therefore inherit genes for whatever trait is preferred

as well the genes for the preference for that male trait (which are only expressed in females). This

process is generally known as the Fisher process (Fisher 1958; Andersson 1994). Linkage

disequilibrium may occur because females carrying genes determining female preference for preferred

7.

male traits (e.g., genes for preferring peacocks with long trains) mate with males carrying the genes

that underlie the male traits that fulfil female mating criteria (e.g., genes for long trains in males). For

example, an artificial selection experiment female guppies were selectively mated with more orange

coloured males and after a few generations it was found that female offspring showed a stronger

preference for males with greater amounts of orange colouring (Houde 1994). Houde (1994) showed

that there is a genetic correlation between orange colour in males and female preference for orange

males, supporting Fisher’s runaway hypothesis. Other studies have shown similar genetic correlations

in sticklebacks (Bakker 1993), fruit flies (Blows 1999), moths Uthesia ornatrix (Iyengar et al. 2002) and

crickets (Gray and Cade 1999). The Fisherian model, however, lacks an explanation for how female

choice initially arose (Kirkpatrick 1987) and, although linkage disequilibrium is often used to define the

Fisher process, the two are not mutually inclusive (Lande 1980; Pomiankowski 1988).

Models encompassing both ‘good gene’ and Fisherian principles (termed the ‘Fisher-Zahavi’

process) are more inclusive and probably more realistic than trying to differentiate between these

models as this distinction is often a matter of how they are defined (Kokko et al. 2006).

1.4.4. The Lek paradox

In species where females receive little from males but sperm (and assuming that indirect

benefits are a relatively weak force in compensating for direct fitness costs), how does female choice

persist (see Kirkpatrick and Ryan 1991)7 The related question of how variation in preferred male traits

persists in a population, despite being selected against by strong directional selection, is known as the

‘lek paradox’ (e.g., Borgia 1979; Taylor and Williams 1982). Genes for preferred male traits should

become fixed in a population; nevertheless there is evidence of additive genetic variance in spite of

direction selection (Houle 1992; Pomiankowski and Möller 1995 ). One explanation is that preferred

male traits are condition dependent and the numerous loci influencing overall condition could shelter

large amounts of genetic variation (Rowe and Houle 1996). Another explanation also assumes that

preferred male traits are condition-dependent, but rejects the notion that the “best” genotype is static

in time or space. Rather, the “best” genotypes vary among environments therefore additive genetic

variation in condition may actually be high (Lesna and Sabelis 1999; Kotiaho et al. 2001; Kokko et al.

2002). Male attractiveness is subject to life-history trade-offs like all other functional traits (Grafen

1990; Kokko 2001), and males change the allocation of resources into attractiveness in response to

their environment (Candolin 2000; Badyaev and Qvarnström 2002; Hunt et al. 2004b), but due to

genotype by environment interactions allocation strategies may differ among genotypes.

8.

It is important to note that direct and indirect benefits are often treated as mutually exclusive

reasons for choosing mates, but a female can receive any mixture of the two benefits (Cordero and

Eberhard 2003; Kokko et al. 2003). As long as the sum of the benefits outweighs the costs, the

behaviour of female choice will persist (i.e. female choice ultimately results in a greater number of

descendents), otherwise it would be more advantageous to mate randomly.

1.4.5. Strength of indirect selection

Indirect selection, however, is often thought to be a weak evolutionary force in comparison to

direct selection on mating preferences (Kirkpatrick 1996; Kirkpatrick and Barton 1997; Houle and

Kondrashov 2002) but the relative contribution of direct and indirect selection has not been quantified

(Hall et al. 2000) though there have been some recent attempts (Arnqvist and Rowe 2005). Empirical

data suggest that the heritability of fitness in nature is generally low (Burt 1995; 2000). In one of the

few field studies to measure additive genetic variation of fitness, Merilä and Sheldon (2000) found no

heritability of lifetime reproductive success in male collared flycatchers Ficedula albicollis. Möller and

Alatalo (1999) reviewed 22 studies showing viability benefits to offspring of attractive males and found,

on average, that 1.5% of variation in viability was explained by male traits preferred by females. This

implies that the influence of ‘good genes’ on female choice is reasonably slight, though it appears to

be pervasive across taxa.

1.5 Sexual conflict

Strict genetic monogamy generates the same reproductive interests for both sexes, however

most species are to some extent sexually promiscuous (reviewed in Birkhead and Möller 1992) and

the lack of monogamy allows for divergent interests between mates. An alternative theory to the

traditional models of mutualistic evolution generating female choice incorporates sexual conflict (the

divergence of reproductive interests between the sexes over mating). Sexual conflict theory covers the

gamut of direct costs on females resulting from male manipulation to maximise his own reproductive

success (Chapman et al. 2003; Arnqvist and Rowe 2005).

Direct costs of sexual antagonism arise from males who evolve specialised means of enticing

females to mate (by expressing high levels of ‘stimuli’), or ways to increase their fertilisation success

at the expense of lowering a female’s lifetime reproductive output. These direct costs of sexually

antagonistic coevolution have been demonstrated to arise by a variety of mechanisms such as the

spiked intromittent organ of the bean weevil Callosobruchus maculatus that wounds females during

intromission: when females are prevented from kicking males and terminating copulations, they incur

9 .

even more damage (Crudgington and Siva-Jothy 2000). There is also evidence in the bed bug Cimex

lectularius of insemination by piercing the female body wall with modified male genitalia that result in

females remating at suboptimal rates and thereby reduces their longevity (Stutt and Siva-Jothy 2001).

In common dungfly Sepsis cynipsea, copulating pairs have long, violent precopulatory struggles,

which may be caused by females trying to avoid injuries inflicted by males (Blanckenhorn 2002). The

male intromittent organ damages the female reproductive tract and copulations greatly increases the

likelihood of female death. Aggression towards females is frequently seen among primates in

promiscuous mating systems, and in chimpanzees sexual coercion to constrain female choice and

gain higher mating success is the most probable function of male aggression toward females (Muller

et al. 2007).

The best studied case of the occurrence of male manipulation of female reproductive

physiology is the reduction in female lifespan in fruitflies Drosophila melanogaster due to harmful

proteins transferred in seminal fluid (Chen et al. 1988; e.g., Chapman and Partridge 1996; but see

Rice 1996; Holland and Rice 1999; Civetta and Clark 2000; reviewed in Chapman 2001). Seminal

fluids reduce the competitive ability of sperm from other males, thereby increasing male fertilisation

success (Harshman and Prout 1994). Additional evidence for sexual conflict in D. melanogaster is that

when females are prevented from coevolving with males, males become even more damaging to

females (Rice 1996; see also Holland and Rice 1999). This leads to the next aspect of sexually

antagonistic coevolution: evolution of female resistance to male manipulation.

A recent review by Wedell et al. (2006) examined which aspects of life histories are most likely

to be most influenced by sexual conflict. Conflict is inherent in all aspects of investment in

reproduction from gamete production to parental care. Even the expression of genes is under conflict

between the sexes: intralocus conflict is when the same allele has opposite effects on the fitness of

the sexes (Fisher 1930; Lande 1980). For example, males benefit from narrow pelvises that increase

locomotion performance while females benefit from broader pelvises for the purpose of childbearing

(Rice and Chippindale 2001). Therefore, genes for pelvic width are under sexually antagonistic

selection which acts to stabilise evolution on the trait, and also selects for sex-limited expression (Rice

1984) either through modifiers or translocation of alleles to the sex chromosome. This idea was tested

experimentally with D. melanogaster. Prasad et al. (2007) showed a marked increase in male fitness

and sexually dimorphic trait expression over 25 generations of limited genome-wide gene expression,

but when these male-evolved genomes were expressed in females, their fitness displayed a nearly

symmetrical decrease.

10.

Unlike intralocus conflicts, interlocus conflict cannot be solved through sex-limited expression.

Conflict arises from the evolutionary advantage of individuals that manipulate their mate to maximise

their own reproductive output. Genotypes that influence mates to increase their investment in the

current reproductive event will be selected for (Lessells 1999). Interlocus conflict between the sexes

arises from each sex having a different optima in terms of life history aspects of offspring production,

such as mating rate. Sexual conflict over mating is well documented: females have lower optimal

mating rates than males (Arnqvist and Nilsson 2000) as mating can be costly (Daly 1978). Males can

gain additional matings in several ways: (1) offering direct benefits [e.g. nutrients in ejaculate (Vahed

1998)]; (2) offering indirect benefits (Kokko et al. 2003); (3) exploiting sensory biases [orange

colouration in guppies (Rodd et al. 2002)]; (4) imposing costs to resisting matings [e.g. cost to females

of dislodging males in water striders (Watson et al. 1998), and; (5) by physically forcing copulations

with females [e.g. grasping and anti-grasping structures in water striders (Arnqvist and Rowe 1995).

Conflict exists over the timing of remating as well as remating rates (reviewed in Wedell et al. 2006).

Conceptually interesting, these strategies offer an alternate perspective on the evolutionary

drivers of female choice. Female preference for not mating is often termed female resistance, although

this is still a form of choice {sensu Wiley and Poston 1996) that leads to direct selection on a subset of

males (Holland and Rice 1998). In this scenario, female preferences simply act to reduce the number

of times females mate favouring the more persistent or manipulative males (Gavrilets et al. 2001;

Rowe et al. 2005). In this sense, sexual conflict is intrinsically driven by the same forces as the direct

benefits model of female mate choice. Mating preference in both models leads to an increase in

female reproductive output and sexual conflict is still inherent in the direct benefits model (some males

provide more benefits than others). The lost opportunity of gaining any extra benefit from mating

selectively is functionally the same as reducing a cost of mating unselectively.

1.6 Male-male dominance

In most taxa, larger males are more likely to win fights (spiders: Kotiaho et al. 1997; e.g. birds:

Hagelin 2002; lizards: Lopez et al. 2002; Reichard et al. 2005). It is generally assumed that stronger,

more dominant males are better quality mates (Berglund et al. 1996). One possible direct benefit of

mating with these males is that they are more likely to protect the female during and after mating.

Another benefit is that they may provide access to superior resources (e.g., better quality territories in

birds). In addition, there is a potential genetic benefit if traits that increase success during male-male

competition are heritable (Cordero and Eberhard 2003).

1 1 .

Although there is a mating bias favouring larger males in a variety of animal taxa, including

many insects (reviewed in Choe and Crespi 1997), the assumption that females prefer larger,

presumably more dominant, males has been challenged (Qvarnstrom and Forsgren 1998). A small but

growing number of studies report no correlation between male fighting ability and attractiveness

(insects: Moore and Moore 1999; Moore et al. 2001; frogs: Morrison et al. 2001; birds: Andersson et

al. 2002; lizards: Lopez et al. 2002; fish: Wong 2004). This could occur because dominant males

impose direct costs on females making them less attractive as mates. For example, they may provide

less or lower quality parental care (Forsgren 1997; Wong 2004), increase the risk of female injury

while mating (Leboeuf and Mesnick 1991), be more likely to transmit diseases (Freeland 1981) or be

sperm depleted (Pitnick and Markow 1994; Preston et al. 2001). There may also be genetic costs if,

for example, male size or dominance is negatively genetically correlated with female fitness, leading to

the production of lower quality daughters, i.e. inheriting sexually antagonistic genes (Chippindale et al.

2001). It is also possible that females do not prefer dominant males because dominance has no effect

on female or offspring fitness, or because there are other traits, uncorrelated with fighting ability, that

are better predictors of a male’s effect on female fitness. Ultimately, the relative magnitude of any

direct effects on female lifetime fecundity and indirect effects on net offspring fitness will determine

whether females should prefer to mate with dominant males (Fedorka and Mousseau 2004).

1.7 Fish as models for parental care

One trait that females may use for selecting their mates is the quality of the male parental care

that they will provide (Forsgren 1997; Wong 2004). Parental care is any form of behaviour that

increases the survival or fitness of that parent’s offspring (Clutton-Brock 1991). Parental care exists in

many forms, from preparing nests [e.g., male common gobies, Pomatoschistus micropa (Nyman

1953)], producing larger eggs [e.g., the skipper, Parnara guttata guttata, (Seko and Nakasuji 2004)],

caring for eggs [e.g., incubation in birds (Hanssen et al. 2003) and mouth-brooding in fish

(Oppenheimer 1970)], to caring for offspring [e.g., feeding nestlings (Drent and Daan 1980b)], and

fully independent young [e.g., Kloss’s gibbon, Hylobates klossii (Tilson 1981)].

Fish present highly suitable but comparatively rarely utilised model systems for studies of

parental care. Fishes are the most numerous and varied of the vertebrates, with over 28 600 species

listed by Fishbase (2004). Despite this abundance, fish are hugely under-represented in behavioural

studies. Studies on birds make up 67% of papers on the two taxa, yet there are three times as many

species of fish as there are of birds (Amundsen 2003). A lot less is known about the patterns of mate

choice and parental care in fish compared to birds. A series such as Birds of the World (del Hoyo et al.

12.

1992-2003) summarise comprehensive knowledge about almost all extant bird species, while there is

nothing comparable for fish. Fish biologists must either stick to a few well-known fish species, or

spend a lot of time learning about the fish they are studying. There are a few reasons for this: (1)

aquatic habitats are difficult to conduct research in; (2) many studies where the focus is on monitoring

variation among individuals require closed, preferably small, populations but aquatic habitats are

usually continuous; and (3) fish are difficult to mark individually.

In teleost (bony) fish, 57% of freshwater breeding families show parental care of eggs or

young (Baylis 1981). Within ray-finned fish, 20% of the 400+ existing families have species that

display some form of parental care (Blumer 1979; 1982). Fish are an interesting taxa for parental care

research because they show a wide range of often dynamic care patterns ranging from no-care, to

uniparental, paternal and maternal care (Gross and Sargent 1985; Reynolds et al. 2002). Among fish,

the majority of external fertilisers (76%) display male parental care which usually involves defence of a

territory containing eggs from more than one female (Gross and Sargent 1985).

A recent study by Mank et al. (2005) reviewed the phylogenetic data for the whole ray-finned

fish group (Actinopterygii). Mank et al. found parental care in 31% (62 of 174) of families, and in 25%

(49 of 193) of external fertilising (ovuliparous) fishes in the group. They showed that all forms of

parental care (biparental, maternal and paternal) have arisen repeatedly and independently during

Actinopterygii evolution. Paternal care arose from external fertilisation, and maternal care arose via

internal fertilisation from external fertilisation. Foundation phylogenetic studies of the evolution of

parental care in a few specific groups of fish (Gross and Sargent 1985) and anuran frogs (Weygoldt

1987) proposed a stepping stone model of the evolution of care from external fertilisation to paternal

care, biparental care and finishing with female-only care. The results from Mank et al (2005) contradict

these stepping stone models, however, and this is not the first study to do so (Goodwin et al. 1998;

Summers et al. 1999).

1.8 Parental care behaviours

Egg guarding is the most common form of care in fish, followed by nest building and then egg

fanning (Blumer 1979). Reduced egg predation or increased hatching success are probably the two

main benefits of male guarding (Baylis 1981). In teleosts, egg guarding is associated with relatively

large egg size and comparatively low fecundity possibly because the longer development period of

larger eggs favours guarding to reduce mortality. In fish, fanning is the most studied parental care

behaviour as oxygen availability is the predominant factor affecting embryos development and survival

(Davis 1975). Embryos subjected to low oxygen (hypoxic) conditions suffer reduced development rate

13.

(Kinne and Kinne 1962; Mihelakakis and Kitajima 1994) and lower survivorship (Dudley and Eipper

1975; Spoor 1984) and egg fanning primarily functions to provide more oxygen for developing

embryos (Tinbergen 1951; van lersel 1953; Sevenster 1961). At low oxygen levels, males will increase

their fanning rate (Reebs et al. 1984; Jones and Reynolds 1999; Green and McCormick 2005) but the

costs of care such as fanning also increase (Hale et al. 2003; Lissaker et al. 2003). As conditions

change and the cost to benefit ratio changes, males often respond by eating all the eggs especially if

they are tending a small clutch (Lissaker et al. 2003). Parents do have ways to alleviate these costs,

such as building nests with larger opening for increased ventilation under low oxygen conditions

(Takegaki and Nakazono 1999; Lissaker and Kvarnemo 2006). It is therefore clear that increasing

oxygen availability to offspring due to fanning by a parent is very important for the offspring’s

development and survival (Zoran and Ward 1983; Kramer 1987; Takegaki and Nakazono 1999;

Lissaker et al. 2003).

Studies measuring filial cannibalism (eating one’s own offspring) show that this behaviour

appears to be common among paternally caring fish (Fitzgerald 1992; Hoelzer 1995; DeWoody et al.

2001; Manica 2004). Partial filial cannibalism has been suggested to have evolved as an adaptive trait

that helps parents to recover the energetic costs of parental care, assuming parents are food-limited

and offspring represent an adequate alterative energy source (Rohwer 1978). Complete filial

cannibalism may have evolved to allow parents to compensate from ‘doomed’ reproductive events

(Fitzgerald 1992; Manica 2002). Studies on Cortez Damselfish Stegastes rectifraenu (Hoelzer 1992)

and gobies Pomatoschistus microps (Kvarnemo et al. 1998) have shown that supplementary feeding

reduces the rates of filial cannibalism, supporting the claim that parental care is costly and that partial

filial cannibalism helps to alleviate these costs. That filial cannibalism is a means to obtain additional

provisions is not an undisputed explanation though. Other studies have shown no decrease in filial

cannibalism by males provided with supplementary food [e.g., in sticklebacks (Belles-lsles and

Fitzgerald 1991), fantail darters (Lindstrom and Sargent 1997), river blennies (Vinyoles et al. 1999),

and sand gobies (Kvarnemo 1997)].

The duration and frequency of parental care behaviours has been shown to vary with

changing parental care cost-to-benefit ratios. The incidence of filial cannibalism, for example, has

been studied by Manica (2004) in the scissortail sergeant Abudefdul sexfasciatus. The cost of care

was reduced by supplementary feeding, and the apparent benefits were reducing by changing the

perceived relatedness of the male to the offspring by showing the caring male a video recording of

rival males to simulate intrusions into the parent’s nest. Supplementary feeding (lowering the cost of

14.

care) reduced the rate of filial cannibalism, while decreased certainty of paternity (reduced benefit of

care) increased the rate of filial cannibalism.

1.9 Variation in parental care

A foundation assumption of studies on the evolution of parental care is that caring for offspring

reduces the survival or future reproductive success of parents (for a comprehensive discussion see

Clutton-Brock 1991). Models of parental care assume that the cost in expenditure in a current

reproductive event reduce the survival or future reproductive success of parents, despite increasing

the current offspring’s reproductive value (Williams 1966a; 1966b; Schaffer 1974b; 1974a; Pianka

1976; Carlisle 1982; Sargent and Gross 1985; 1986; Winkler 1987; Curio 1988; Montgomerie and

Weatherhead 1988). Conversely, saving resources for future reproduction reduces the fitness of the

present offspring but increases subsequent reproductive success. Individuals are expected to

maximise their overall reproductive success by trading off investment between current and future

reproductive events (Winkler 1987). For example, when dissolved oxygen levels decrease, the cost to

ratio benefit changes as care becomes more costly (Hale et al. 2003; Lissäker et al. 2003), and males

often respond by abandoning their current reproductive investment (eating all the eggs). Although

parents would be expected to adjust parental care to maximise their own fitness, to predict variation in

parental care accurately there must be an understanding of the costs and benefits associated with

parental care under different situations.

1.10 Costs and benefits of parental care

Parental care is demonstrably costly. There are energetic costs to building a nest or burrow to

house offspring, for example, black-billed magpies Pica hudsonia have to increase their daily intake by

0.7% - 1.0% to cover the energetic costs of nest construction (Stanley 2002). Although this cost is

relatively small, producing eggs is very costly; female black-billed magpies egg laying is estimated to

require a full 23% of the daily energy expenditure (Stanley 2002). Caring for eggs is also costly, a

clutch-size manipulation experiment in female common eiders Somateria mollissima showed that

females of low quality were unable to increase incubation effort and were more likely to abandon the

nest (Hanssen et al. 2003). On the other hand, females of higher quality apparently had the capacity

both to increase incubation effort and investment in brood care (Hanssen et al. 2003). Male

cardinalfish (Apogonidae) care for their eggs by keeping them in their mouths until they hatch

(Thresher 1984). Males therefore do not feed during this time (Okuda and Yanagisawa 1996) and

mouth-brooding has been found to severely reduce the male’s ability to take up oxygen at reduced

15 .

dissolved oxygen levels (Östlund-Nilsson and Nilsson 2004). Caring for young after they hatch may be

even more costly, feeding nestlings required quadrupling of the basal metabolic rate in five species of

bird (Drent and Daan 1980b). These examples all highlight the importance of body condition as a

factor that could affect the quality of parental care an individual can provide.

In most species, the costs of care are high and for it to have evolved there must, therefore, be

appreciable benefits in terms of improving offspring survival or performance (e.g., in situations of high

predation risk, under high competition for resources or under harsh conditions). For example, female

treehoppers Publilia concava exhibit a range of guarding durations, and females that remained to

guard eggs had fewer and smaller future broods than those that abandoned their offspring, suggesting

a high cost to future reproductive output (Zink 2003). On the other hand, experimentally removing the

female resulted in loss of half of the eggs by predation. Estimates of lifetime fecundity of females that

abandon eggs early versus remain to guard eggs showed roughly equivalent levels of fitness.

Females may therefore only choose to guard when their eggs are under immediate high predation risk

(Zink 2003). Similarly, in the burying beetles Nicrophorus vespilloides parents provide elaborate

parental care to their offspring by guarding a resource from competing conspecifics that has a major

beneficial effect for offspring. Parental beetles bury a small vertebrate carcass (which constitutes the

sole food source for the larvae) and this complex parental care immediately prior to larval hatching

greatly improved offspring survival rates. In addition, continued parental presence for several days

after eggs hatch, during which adults regurgitate pre-digested carrion to their young (Fetherston et al.

1990), also improved larval growth (Eggert et al. 1998).

1.11 Honest Signalling

Parental care can be seen as a direct benefit of female choice, and if a male can signal his

quality as a caregiver, he may increase his mating and reproductive success. A female who uses that

signal to choose a high quality male will also gain from this choice. If males of inferior quality,

however, also displayed this signal they stand to gain from the increase in mating success but females

would suffer from the decreased parental care. The question is then, in the face of these conflicting

interests between signallers and receivers, can signals of quality (care or otherwise) be honest?

Sexual displays (or signals) are under selection by female choice and many studies have

shown a positive correlation between sexual displays and either parental investment or resources

(e.g., Linville et al. 1998; Candolin 2000; Senar et al. 2002; Voltura et al. 2002; Kolm 2004; Halupka

and Borowiec 2006). Other studies show the contrary result, in that preferred or actively courting

males actually provide less parental investment (e.g., Qvarnström 1997; Wong 2004; Mitchell et al.

16.

2007) or that there is no relationship between parental investment and a sexual display signal (e.g.,

Mountjoy and Lemon 1997; Smiseth et al. 2001).

Secondary sexual characteristics are expensive, as already discussed, and the “handicap

principle” suggests that only males of high quality and in good condition can bear the cost of

displaying them, therefore ensuring that sexual advertisement will be honest (Zahavi 1975). The

requirement that signalling is costly therefore appears essential for signalling of quality to be honest

(Getty 1998). Some studies have shown, however, that costly advertisement does not always lead to

honest signals. Parasitised male Drosophila melanogaster with reduced life expectancy increased

their courtship effort (Polak and Starmer 1998) while three spined sticklebacks in poor condition

displayed greater nuptial colouring that their higher quality counterparts. This can come about when,

at the end of a male’s lifetime, future reproductive chances become diminished and the trade-off

between current and future reproductive is diminished. This terminal effort in signalling could lead to

temporary dishonest signalling, although ‘on average’ across a lifetime the positive correlation

between signal expression and male quality persists (Kokko 1998b). There is the possibility, however,

that this terminal energy expenditure in signalling also correlates with an increase in expenditure on

parental care, and the signal then remains honest in terms of signalling parental investment.

There are two hypotheses that model whether or not signalling will be an honest predictor of

parental quality. The good parent hypothesis (Heywood 1989; Hoelzer 1989) suggests that male

secondary sexual characteristics will signal a male's ability to provide parental care due to selection

imposed by female choice and therefore predicts honest signalling. The ‘differential resource

allocation’ hypothesis predicts a reduction in care from attractive males because females will increase

their parental investment to obtain or retain an attractive mate (Burley 1986). In a key model, Kokko

(1998) shows that the predictions of both models can occur and it is the extent to which males stand to

gain from additional matings that will decide on the direction of signal honesty. If the benefits of

additional matings are only marginal, signals are expected to honestly convey genetic and phenotypic

(parental care) quality. If the gains from additional matings are increased, males are likely to allocate

greater resources to displaying the signal and find more mates, and provide less care. More generally,

the effort that males invest in parental care is often negatively associated with mating opportunities

(Westneat et al. 1990).

As an aside, the evolution and maintenance of honest signaling may be partially affected by

condition. Mate preferences for honest signals should be more beneficial for high quality females if low

quality females have less to gain from discrimination (Cotton et al. 2006b). Hypothetically, in a species

in which male display rate honestly signaled male investment in parental care, high quality females

17.

who can produce more offspring than the average male can care for should prefer well-ornamented

mates, as this will directly increase their fitness. In contrast, if low quality females produce few

offspring that can be adequately cared for by an average male, then such females should mate at

random, and avoid paying the costs of mate choice where there is a much smaller benefit (Cotton et

al. 2006).

Signals of parental care need not necessarily be sexually selected traits. Females might

directly observe cues of parenting instead of relying on the honesty of correlated traits. Studies have

been conducted that shown females prefer males of high parental quality, rather than basing their

choice on male dominance or size (e.g., sand gobies Forsgren 1997) although what cues females

base this choice on isn’t always clear. Three spined sticklebacks have exclusive paternal care and

males have larger pectoral fins than females, probably to facilitate better care for eggs when fanning.

The size of a male’s pectoral fin is condition-dependent and females could use fin size to directly

select males of higher parental quality (Bakker and Mundwiler 1999), although this still leaves open

questions about fanning rate which also affects the quality of the care provided.

In some species, males invest a greater amount into parental care than females, and where

nesting sites or territories are limited, the operational sex ratio becomes skewed toward females.

Termed ‘sex role reversal’ (Gwynne 1991; Vincent et al. 1992), this lead to a situation where females

compete for mates and males become choosy. This has been demonstrated in many species (e.g.,

pipefish, Silva et al. 2006; and blennys, Lengkeek and Didderen 2006; Shibata and Kohda 2006). So

do females display honest signalling as well? Some studies show they do (Möller 1993; Langmore et

al. 1996; Svensson et al. 2006) and some that they do not (Hill 1994; Telia et al. 1997).

1.12 Foraging: maximising energy gain

With so much literature focusing on energetically expensive activities such as presenting and

maintaining sexually selected traits, mate searching, interspecific competition, mate choice, mating,

and parental care, it is logical to examine means by which animals obtain energy for these activities.

The efficiency with which individuals gain energy is of immense importance and affects their

competitiveness in competition for access to mates (e.g., dominance struggles) and the expression of

traits that are condition-dependent (e.g., honest signals of quality)

Different habitat structures present animals with differences in food density and associated

food values, such as search times. As discussed above, several species of generalist feeding fish

have been shown to selectively choose food based on their size (e.g., Ivlev 1961; Galbrait 1967;

Brooks 1968; Hall et al. 1970; Munk 1992; Forrester et al. 1994; Luo et al. 1996; Graeb et al. 2006;

18.

Hyvarinen and Huusko 2006). Food size is important to fish growth and may studies demonstrate a

positive relationship between the two (Leeren 1958; Parker and Larkin 1959; Paloheim and Dickie

1966; Graeb et al. 2004; Harter and Heck 2006; Persson and De Roos 2006). Food size is also

important when trying to maximise energy gain, as optimal allocation time spent searching for and

handling prey will change with the energy return for different sized food items

Microhabitat choice (specifically substrate discrimination) is one aspect of patch choice

behaviour that was the subject of a recent study by Webster and Hart (2004). Webster and Hart

(2004) presented three spined sticklebacks Gasterosteus aculeatus simultaneously with food items on

simple and complex substrates, repeating the experiment with different densities of food items. The

sticklebacks showed a marked preference for complex microhabitats when food densities were equal

between substrates, and when density was greater on the complex substrate. Webster and Hart

(2004) cite the link between increased substrate complexity with higher macroinvertebrate densities as

the cause. Increased structural complexity, however, increases the handling and searching times of

smaller prey and this will decrease the associated value of that food item and therefore the net intake

of energy for that patch. I wanted to emulate this study to see if this result was repeatable and if the

decrease in food value from a more complex microhabitat would yield a different result in a different

species.

19.

1.13 Aims of this study

The overall aims of my study are:

1. Investigate what female Mogurnda mogurnda prefer in relation to male size and fighting

ability. Fighting ability (or dominance) is often automatically regarded as being a predictor of female

mate choice but recent papers do not support this claim. My study is designed to add to the growing

list of literature that document whether or not there is a female preference for dominant males when

male-male competition is controlled for.

2. To compare female mate preferences between traditional association preference tests and

latency to mating (spawning time) trials. Recent studies suggest that association preference tests

are not necessarily robust, when the results are compared to latency to mating tests, either preferred

characteristics are no longer preferred or different characteristics become indicators of male

attractiveness.

3. To investigate whether male M. mogurnda display honest signalling of their parental quality,

and if females chose males based on these characteristics. To do this I looked for any correlations

between male size, dominance or attractiveness (as defined by female preference trials) and

parental care.

4. To study a relatively new aspect of foraging behaviour, substrate discrimination. I wanted to

see if individuals showed preference for the greater potential for food presented by the higher

incidence of interstitial spaces in “complex” substrates. By comparison, “simple” substrates hold less

potential for hiding food items. I wanted to see if M. mogurnda showed a preference for foraging

grounds based on these topographical differences.

20.

1.14 Study species

Mogurnda mogurnda, commonly known as the northern trout gudgeon, is widely distributed

across northern Queensland and the Northern Territory (Allen et al. 2002). They can be found from

Mossman (QLD) to Mitchell River (WA), in the Lake Eyre drainage, and in some areas of southern

Papua New Guinea (Fig. 1.1.1). M. mogurnda inhabits slow moving waters in rivers, creeks and

billabongs, congregating around vegetation or rocks. Adult fish prey upon insects, crustaceans,

worms, molluscs, fishes and plant materials.

With wide physiochemical tolerances, M. mogurnda can withstand short periods of low oxygen

levels, water temperatures from 5 to at least 32°C and salinities up to 10,000 parts per million.

Growing to a maximum size of 17cm, their appearance is very similar to that of the better-known

purple-spotted gudgeon Mogurnda adspersa. Dark brown dorsally and lightening to a cream on the

belly, M. mogurnda has dark bars running vertically with numerous reddish spots featuring prominently

on the body and head Fig. 1.1.2). Three diagonal bands of spot run from under the eye across the

cheek, and spots featuring on the dorsal, caudal and anal fins. Somewhat non-descript when stressed,

M. mogurnda displays iridescent blues and purples when in breeding colours.

M. mogurnda spawns during the rainy season (November to March). Sexual dimorphism is

displayed during the breeding season; the male urinogenital papilla is pointed and may attain an

intense blue colouration, and in females the papilla is shorter and broader with a fringed margin. I

used this difference to sex individuals in my study. Spawning involves the adults swimming closely

together and the female produces several batches of 100-500 eggs that are deposited on rocks or

logs. The demersal adhesive eggs are attached, in a cluster of around 50mm in diameter, to the

substrate by small threads and waft in the current. The males guards and fans the eggs until hatching,

which anecdotal evidence suggests takes between 8 and 10 days in the wild, although they will hatch

much more rapidly in aquaria (on average after about 5 days).

21 .

Figure 1.1.1 The distribution of Mogurnda mogurnda across Australia is highlighted across northern

Australian and the Lake Eyre drainage. They are also found in southern Papua New Guinea (not

shown) (NFA, 2006).

22 .

Figure 1.1.2 Male Mogurnda mogurnda guarding his egg mass in an aquarium.

23.

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46.

CHAPTER 2 Mate choice in the northern trout gudgeon

(Mogurnda mogurnda)

2.1 Introduction

2.1.1. Female mating preferences

In many taxa, females appear to choose between potential sexual partners. How and why mate

choice evolves remains elusive in most cases (Andersson 1994). In general, mating can be costly (Daly

1978), and mate choice often aggravates these costs. The costs of mating include suffering an increased

risk of predation (Sakaluk and Belwood 1984; Magnhagen 1991), and time and energy costs while

searching for males (e.g., Alatalo et al. 1988; Gibson and Bachman 1992). The risk of predation can also

be greater on copulating pairs, sexually transmitted disease can have negative fitness consequences, and

mate searching and copulation may hinder activities unrelated to mating such as foraging (e.g., Keller and

Reeve 1995; Jivoff 1997).

Discriminating among males increases the costs associated with mating and, in the absence of

benefits, should lead to selection against female mating biases (Bulmer 1989). For female choice to

persist there must be benefits to compensate for any costs associated with mate choice, otherwise it

would be more beneficial to mate randomly (Friberg and Arnqvist 2003). One of the most straightforward

explanations for the evolution of female choice is that it results from evolutionary processes that favour an

increase in female lifetime reproductive success (e.g., increased lifespan or increased egg production)

compared to mating non-randomly (Heywood 1989; Hoelzer 1989; Price et al. 1993; Kirkpatrick 1996;

Iwasa and Pomiankowski 1999).

2.1.2. Life history traits and female mating preferences

Recent studies have examined sexual selection from a functional perspective, with a particular

focus on the correlations between physiological performance, secondary sexual traits, male-male

competition and female choice. In a recent review, Lailvaux and Irschick (2006) summarised this emerging

field of study and asked two key questions: Are males who enjoy increased mating success also of high

physiological or phenotypic quality? And, are these males consequently good fighters? Lailvaux and

47 .

Irschick (2006) define two physiological measures; whole organism performance capacity and

physiological state. Whole organism performance capacity (“performance”) encompasses how well an

individual performs an ecologically relevant task, e.g., how fast a fish can swim or even how many

offspring a female can produce in a year (Irschick and Garland 2001). Physiological state (“state”) refers to

the measure of the physiological processes of an individual (e.g., metabolic rates or muscle function). In

sexual selection studies, a male’s “condition” is often an important variable and condition is said to be

encompassed within physiological state in the review.

Male secondary sexual characteristics are generally considered to be costly to produce and/or

maintain (Kotiaho 2001), particularly male vocalisations. For example in frogs and toads, calling males

have a metabolic rate exceeding a factor of 100-220% of the baseline rate (see Gerhardt 1994) and this

huge investment in energetics may reduce their future reproductive encounters (McLister 2003). Studies

have also shown that sexual displays are highly sensitive to male condition (Cotton et al. 2004;

Bonduriansky and Rowe 2005). Logically then, males in better condition can afford to invest more into

sexual displays or secondary sexual characteristics but this does not mean that their physiological state

(post-investment) will be positively correlated with sexual display (Grafen 1990; Kokko and Monaghan

2001; Hunt et al. 2004a; Tomkins et al. 2004). Male may need to be in good condition to produce sexual

advertisement but sexual advertisement may trade off against other functional and life history traits.

Recent studies show that males who heavily allocate resources into sexual advertisement suffer a

reduction in other fitness costs, such as survival, and that the optimal returns are sometimes such that the

males will the most resources invest so heavily into sexual displays that they actually have shorter

lifespans (Hunt et al. 2004).

2.1.3. Male dominance and female mating preferences

So are dominant (and assumedly more reproductively successful males) of higher physiological

quality? Physiology has been implicit in some models of male-male competition (e.g., resource holding

potential: Parker 1974) but the underlying physiological basis of why some males are better than others

has rarely been addressed. High metabolic rates are assumed to be a cost of male dominance (Roskaft et

al. 1986; Bryant and Newton 1994; Metcalfe et al. 1995; Whiting et al. 2003) but this may not always be

the case. Subordinate males may be involved in more challenges than dominant males and therefore

forced to maintain a higher metabolic rate (Sloman et al. 2000). Dominant males may not even suffer

higher metabolic costs of fighting. For example in cichlids, there are relatively higher levels of lactate and

48 .

other end product in males that lose fights (Neat et al. 1998). Some performance measures have been

shown to positively predict success in male-male competition, such as locomotor performance in lizards

(Robson and Miles 2000; Perry et al. 2004). In male sticklebacks, muscle condition is positively linked to

fighting ability (Guderley and Couture 2005). Males with higher energetic reserves are more likely to be

successful in male-male interactions in several animal taxa, such as insects (Marden and Waage 1990;

Plaistow and Siva-Jothy 1996; Blanckenhorn et al. 2003; Kemp and Alcock 2003), birds (Petrie 1983) and

fish (Chellappa and Huntingford 1989; Neat et al. 1998).

Weapon size is often a good predictor of fight outcome. For example, male dung beetles with

larger horns are more successful in male-male interactions (Pomfret and Knell 2006). Males have the

opportunity during fights to assess a rival’s horn size (Pomfret and Knell 2006) and probably use that as

an indicator of their fighting ability. Females have also shown preferences for to male traits correlated with

dominance, such as colouration in three spine sticklebacks Gasterosteus aculeatus (Candolin 1999a) and

body size in Japanese medaka Oryzias latipes (Howard et al. 1998). In fish, there is a wide literature

showing females prefer larger males in species that show biparental or paternal care (Downhower and

Brown 1980; Noonan 1983; Keenleyside et al. 1985; Goto 1987; Bisazza and Marconato 1988; Cote and

Hunte 1989; Rogers and Barlow 1991), but although often assumed to, females do not always prefer

males that are better fighters (e.g., Moore and Moore 1999; Reichard et al. 2005; but see Wong and

Candolin 2005). Overall, there is a large variation across taxa in the fitness outcomes for females of

mating with dominant males (Qvarnstrom and Forsgren 1998; Moore et al. 2001; Wong and Candolin

2005).

There is evidence that females prefer males with increased performance capacities. For example,

female guppies prefer male ornaments that are correlated with swimming ability (Nicoletto 1991; 1993;

Kodric-Brown and Nicoletto 2005), although interestingly there was no evidence of indirect genetic

benefits in the form of increased performance in offspring (Nicoletto 1995; Evans et al. 2004). On the

other hand, there was no documented female preference for higher performing males in the lizard Anolis

carolinensis (Lailvaux and Irschick 2006). Insufficient data prohibits any firm conclusions as to general

trends, however, and this field of study needs to be developed further.

Female choice might, however, select for males in better physiological condition, as predicted by

the handicap hypothesis (Zahavi 1975) and this trend is prevalent across taxa. In some fish species, only

males in good condition are able to court females in fast water (Takahashi and Kohda 2004; Kodric-Brown

and Nicoletto 2005). In birds, comb size in red jungle fowl is heritable, correlated with an index of (Parker

49.

and Garant 2004) condition and a trait used as a mate choice cue (Parker and Ligon 2003). In insects,

yellow dung flies with relatively higher lipid and glucose levels achieve higher mating success

(Blanckenhorn et al. 2003). Female choice may indirectly select for males of good physiological quality

and thereby also select for condition-dependence of male traits (Bonduriansky and Rowe 2005).

2.1.4. Parental Care and Female Mating Preferences

Another aspect of male performance that female choice has been shown to select for is parental

care. In fish, females have been show to prefer many traits, such as courtship (Knapp and Kovach 1991;

Knapp and Warner 1991; Karino 1995), nest characteristics (Hoelzer 1990; Kvarnemo 1995; Ostlund-

Nilsson 2001), number of eggs in a nest (Kraak and Groothius 1994; Forsgren et al. 1996; Goulet 1998)

and the incidence of filial cannibalism (Goto 1993), that are possible predictors of parental competence

and might provide an honest signal of male parental care. Some studies have even found that females

directly prefer males who are better fathers (Forsgren 1997; Wong 2004; Lindström et al. 2006). Courtship

rate has been shown to be both preferred and positively correlated with increased hatching success in

several studies of species such as the bicolour damselfish Stegastes partitus (Knapp and Kovach 1991;

Knapp and Warner 1991), fifteen spined sticklebacks Spinachia spinachia (Östlund and Ahnesjö 1998),

and pacific blue-eye fish Pseudomugil signifier (Wong 2004). In fifteen spined sticklebacks, increased

fanning beat rate leads to higher egg hatching success but also appears to be energetically expensive as

males who have a greater increase in fan beat rate lost more weight (Östlund and Ahnesjö 1998).

Females prefer males that court more (which is positively correlated to fan beat rate) and as courtship and

fan beat rate are condition-dependent, they appear to provide honest cues for female mating preference

(Zahavi 1975). Honest signalling of male parental care has been demonstrated in several studies (Kunzler

and Bakker 2000; Ostlund-Nilsson 2001; Senar et al. 2002; Takahashi and Kohda 2004; Halupka and

Borowiec 2006), but not in others (Linville et al. 1998; Smiseth et al. 2001; Mitchell et al. 2007) and there

is even evidence of dishonest signals in a few cases (Candolin 1999b).

2.1.5. Measuring female mating preference

The traditional method of determining female mating preference is through simultaneous choice

tests. Ideally these choice tests should exclude male-male interactions, otherwise male-male competition

may be influencing any increased mating success (or a surrogate thereof) for some males. This is

supported by several studies that report dominant males do not enjoy higher mating success when male-

50 .

male competition is removed (Radesater and Halldorsdottir 1993; Nelson and Nolen 1997; Nilsson and

Nilsson 2000; Reichard et al. 2005; Shackleton et al. 2005; Spence and Smith 2006). To control male-

male competition, many studies tether males or place them behind glass or mesh, which also has its

downfalls. Female preferences for specific male traits can differ when the sexes are allowed full or

restricted interactions (Candolin 1999a; Nilsson and Nilsson 2000). Also, in some species males behave

abnormally when tethered (Teleogryllus commodus, pers. obs.). A lack of close physical contact between

the sexes may also deny females access to essential mate choice cues (e.g., cuticular contact

pheromones in the field cricket Gryllus bimaculatus Tregenza and Wedell 1997)] and simultaneously

presenting females with two extremes in male phenotype can also artificially amplify a preference effect

(Wagner 1998). Female preference may be based on more than one male trait (reviewed in Candolin

2003) and a controlled trait might well be correlated with another uncontrolled trait.

Even in species that are better suited to simultaneous choice tests, female mate choice in

preference trials is often only indirectly measured. A relationship between, for example, visual orientation

(Clark and Biesiadecki 2002) or time spent near a male is only assumed to equate to actual mating

success. In a few cases this assumption is tested and supported (Clayton 1990; Witte 2006) but in others

it is not (Gabor 1999; Fuller 2003). There is also evidence of cryptic female choice, associated with rate of

oviposition (Eberhard 1996), differential allocation of eggs (Burley 1986) and post-copulatory sperm

selection (Lifjeld et al. 1994) that needs to be taken into account. The major dilemma therefore is that to

measure actual mating success individuals must interact, but it is difficult to do this without reintroducing

the problematic effects of male-male competition on male mating success.

Another way to measure male attractiveness that resolves these problems is to conduct no-choice

tests (Pilastro et al. 2002). These tests usually measure the time between the introduction of a single male

and female, and when a female acquiesces to mating (latency to mating). Measuring attractiveness as

mating latency has several benefits, females are allowed to base their choice on the entire physical and

chemical cues males offer, and female mating preference can be determined from an actual mating. No­

choice tests measuring mating latency are most often used in fruitfly studies (Hegde and Krishna 1997;

Koref-Santibanez 2001; Gowaty et al. 2002; Yenisetti and Hegde 2003), but they have also been

employed in studies of birds (White et al. 2002), lizards (Tokarz 2002), fish (Houde and Torio 1992;

Blanchfield and Ridgway 1997), and invertebrates (Peters and Michiels 1996; Parri et al. 1998; Bukowski

et al. 2001; Jones and Quinnell 2002). My honours work on the Black Field Cricket (7. commodus) was

one of the few studies to test and confirm that males with a shorter latency to mating in no-choice trials

5 1 .

enjoyed increased longer-term mating success, supporting no-choice tests as an accurate measure of

male attractiveness (Shackleton et al. 2005).

The rate of egg production has been used as another method to assess female mating

preference. Variation in clutch size is one of the few cryptic choice modes employed by external fertilisers

(Eberhard 1996) and has been demonstrate in several taxa (Cote and Hunte 1989; Rintämaeki et al.

1998; Arnqvist and Danielsson 1999; Reyer et al. 1999; Fu et al. 2001; Parker 2003; Smith and Reichard

2005). Adjusting egg volume has also been implicated as a cryptic form of female choice (Kolm 2001), as

well as decreasing the time to spawning (Berejikian et al. 2000). Using egg production as a measure of

female choice, Spence and Smith (2006) have shown that female zebrafish show preference for males by

varying their clutch size and that they do not prefer dominant males.

2.1.6. Aims of this study

In this experiment, I aimed to quantify female mating preferences using the northern trout

gudgeon Mogurnda mogurnda. I tested whether females showed a mating bias and if this was towards

larger (better “condition”) males, or more dominant males. To quantify and record the mating behaviours

of M. mogurnda, I paired males that differed in size and conducted association preference tests with four

females per male pair. For each female, I measured preference variables such as the number of times she

entered a preference zone for each male, and the time spent in close proximity to each male. I then

analysed these variables to determine which characteristics females preferred so that I could then

compare them to any characteristics that might predict the quality of male parental care (Chapter 3).

52.

2.2 Methods

All aquaria were kept at 26° Celsius in climate controlled rooms on a 14:10 hr day: night

illumination cycle. The holding tanks (6’ x 2’ x 2’) where fish were kept between experiments were

connected to sump filters filled with bioballs containing bacteria that break down waste products in the

water. Four holding tanks were used, two for fish before experiments and two for after experiments. The

sexes were housed separately.

2.2.1. Pilot studies on male dominance

As pilot work for this study, I experimented with the best method of measuring male fighting ability

in M. mogurnda and found I was able to qualify relative male dominance but that I was not to quantify it

comprehensively. I wanted to observe and record males engaging in aggressive dominance behaviours to

test the hypothesis that larger males are more aggressive than smaller males. First, I paired males which

visually differed in mass by 5-10% and then I placed them into experimental tanks measuring 2’ x 1’ x 1’

which had two corner filters with carbon and filter wool in each back corner to maintain water quality

during the experiments. A 50% water change was conducted between tests of successive male pairs and

each method described below was conducted with four separate pairs of males.

I placed a pair of males into an experimental tanks, separated by a clear plastic divider that split

the tank into two equal halves with a male on each side. I acclimatised the males for 10 minutes then lifted

the separator and observed them for 10 minutes. I did this for four pairs of males. After 10 minutes of

observation, none of the four male pairs showed any aggressive behaviour towards each other. The

males either ignored each other or engaged in escape behaviour (systematically searching the tank for a

way out). I then repeated the procedure but changed the acclimatisation and observation time to 30

minutes, but still with no success. There were also no observable dominance behaviours when I

acclimatise the males for 30 minutes, one hour, or six hours. They still showed no sign of aggressive

behaviour after I lifted the divider and observed them.

I then tried to acclimatise the males without physically separating them so I acclimatised them

without a divider in the tank and checked on them after 30 minutes, one hour, three hours and six hours.

When I returned after six hours most of the males appeared to have engaged in aggressive or fighting

behaviours. I deduced that a fight had occurred when one male was out in the open and the other was

resting in the corner, often with visual damage to his fins. The fins of the “subordinate” male was often

53.

quite badly harmed, to the point where I had to separate three of the male pairs after three hours.

Observation of pairs showed that the “dominant” male would often chase the other male which quickly

swam to stay away from the dominant male.

The pairs mostly engaged in fighting somewhere between three to six hours, but the fights that

lead to the subordinate males showing the worst damage occurred within the first three hours. I repeated

this method with 12 pairs of males and 11 pairs had engaged in dominance behaviour by the sixth hour

and in all 11 pairs the larger male was the dominant male.

Considering the range and the length of times before the male engaged in dominance behaviours,

I decided that conducting comprehensive male dominance trials was not feasible. The results of the pilot

study which clearly showed that larger males are more dominant is the basis for my assumption that male

size is a good predictor of male fighting ability and dominance in this study on M. mogurnda.

2.2.2. Mate choice trials

I examined mate choice in M. mogurnda by weighing a series of males and then pairing together a

“large” and “small” male who differed in mass by at least 5 g. I randomly assigned four stock females to

each male pair for the duration of the mate choice experiments. Mate choice trials were conducted in

experimental tanks measuring 2’ x T x 1’. They had two corner filters with carbon and filter wool in each

back corner to maintain water quality during the experiments. A 50% water change was conducted

between tests with each female. Each tank had two mesh dividers to create two smaller compartments at

each end and a larger central compartment (Fig. 2.2.1).

On each mesh divider I attached two halves of a plastic tube on either side on the grid to create a

tube that could be used as a possible spawning site and allowed males and females to interact in a

sheltered location. A large and small male from a pair were then placed individually into opposite end

compartment. Males were allowed to acclimate for 10 minutes before the start of each mate choice trial.

The middle compartment was divided into three preference zones; a non-preference zone in the middle

(30 cm wide) and two preference zones at either end adjacent to the male compartments (15 cm wide).

After each mate choice trial, I swapped the males between the end compartments and allowed ten

minutes before the start of the next trial.

At the start of each trial, the female was placed in the centre of the tank under a clear plastic

container with slits in it to allow water flow. The female was then acclimatised for five minutes before the

container was raised. Her position in the tank (e.g., which zone she was in) was monitored for ten minutes

54 .

using the specialised behaviour analysis program JWatcher™ 0.9 from the Animal Behaviour Laboratory,

Macquarie University NSW (Blumstein et al. 2000). I recorded the duration of time spent in each

preference zone (i.e. time spent with each male) as well as the number of times the female left and then

re-entered each zone.

Each pair of males was tested with four females which resulted in four sets of “preference” data

for each male pair. I set an a priori criterion for which experiments were considered successful and which

pairs of males were eligible to proceed to the parental care experiments (see below). I conducted mate

choice experiments until I had obtained a total of 15 pairs of males (n = 60 mate choice trials). I used the

data from these initial mate choice trials to test whether: (1) females prefer larger males; (2) there was a

size-assortative female mating preference; and (3) the strength of preference for attractive males was

consistent for females tested with the same male pair. I then related these characters to male behaviour in

the subsequent parental care experiment.

2.2.3. Preference Criteria

To select pairs of males that differed sufficiently in their attractiveness for the parental care

experiments that followed, I only kept pairs of males that met a set of criteria. There were two

attractiveness categories: “attractive” males were preferred by at least three of the four females; and

“unattractive” males were preferred by none or one of the four female. To determine whether a female

considered one male more attractive than the other, I first excluded the time she spent in the non­

preference zone. I then used the relative time the female spent in each male’s preference zone to

calculate which male she preferred. Relative time was the proportion of time the female spent in a male’s

preference zone relative to the total time spent in both preference zones. If a female spent 66% or more of

her time in the preference zone of one male, I recorded this male as being “preferred” by that female, and

the other as “non-preferred”. If a female spent a more equitable amount of time with each male, the trial

was rejected, another stock female was randomly selected and the trial was rerun. If two females failed to

show a preference for a given pair of males I put all the individuals into the “used” stock tanks and started

again the next day with a new pair of males. When all four females had successfully completed mate

choice trials, I compared their preferences. If three or more females preferred the same male, I deemed

that male as the “attractive” male and the other as the “unattractive” male in the pair. Females that agreed

on which male they preferred were then also returned to the “used” stock tanks.

55 .

2.2 .4 . Statistical Analyses - Mate Choice Analysis

In the analysis of female mating preferences, I considered the following variables:

• The number of visits was the number of times a female entered a male preference zone.

• The total duration was the total amount of time a female spent in a male preference zone.

• The mean duration was the average duration per visit a female spent in a male preference zone.

• The duration proportion was the proportion of time a female spent in a male preference zone

relative to the total duration of the observation period (10 minutes).

• The relative proportion was the proportion of time a female spent in a male preference zone

relative to the time a female spent in both preference zones (excludes the time in the non­

preference zone).

I used Wilcoxon signed ranks tests to analyse whether the mean number of visits, total duration,

mean duration, duration proportion and relative proportion of time differed between large and small males.

For these tests I used the means per male for the four females. Using linear mixed models for each

response variable, I also treated female identity as a random factor nested within male pair identity to test

whether females preferred one male over the other. I modelled all five response variables using male size

and female mass as fixed factors. I also modelled number of visits, total duration and mean duration with

pair number as a fixed factor to see if females were spending more time with some male pairs.

I also conducted an ANOVA to test whether there was a difference in mean female mass among

male pairs. Finally, I tested if there was a significant difference in the mass of females to the males they

were paired with.

56.

Figure 2.2.1 The design of experimental tanks for female mate choice trials. A female was placed into the

centre section, and a large and small male were placed at opposite sides of the tank (the positions of the

males were alternated between trials). The presence of the female in each of the preference zones shown

was recorded using the specialised behaviour analysis program JWatcher™ 0.9 from the Animal

Behaviour Laboratory, Macquarie University NSW (Blumstein et al. 2000).

57.

2.3 Results

Females showed a mating preference for larger males (Table 2.3.1); they spent a greater amount

of total amount of time (Fig. 2.3.1), and a greater mean duration per visit (Fig. 2.3.2) with larger males.

When analysing the data using the mean values from the four females assigned to each male pair,

females spent a significantly greater total amount of time with larger males (Wilcoxon Signed Ranks, Z =

2.101, p = 0.036, n = 15) and tended to stay longer per visit (greater mean duration) with larger males

(Wilcoxon Signed Ranks, Z = 1.931, p = 0.053, n = 15). There was no significant difference in the number

of visits, duration proportion or relative proportion of time between different sized males (P = 0.1 to 0.32).

Using linear mixed models, male mass correlated positively with female preference behaviour

(Table 2.3.2). Females spent more time overall (Fig. 2.3.3), more time per visit (Fig. 2.3.4), and a greater

overall proportion of her time (Fig. 2.3.5) with the larger of the two males. Females also spent a greater

relative proportion of time with the larger of the two males. Using female mass and male mass as fixed

factors and female identity as a random factor, the total duration (F = 14.216, df = 1,117, p < 0.001), mean

duration (F = 6.141, df = 1,117, p = 0.015), duration proportion (F = 8.451, df = 1,117, p = 0.004) and

relative proportion (F = 11.879, df = 1,117, p = 0.001) of time was greater with larger males. There was,

however, still no significant difference between the number of times a female visited each male’s

preference zone.

The level of female preference did not differ significantly across the male pairs (Table 2.3.3).

Using linear mixed models with male pairs as the fixed factor and female identity nested within male pair

as a random factor, there was no difference in the number of visits (F = 0.599, df = 1,45, p = 0.851), the

total duration (F = 0.168, df = 105, p = 1.000) or the mean duration of visits to males (F = 0.892, df =

1,105, p = 0.569) across male pairs.

Mean female mass did not differ significantly across the male pairs (F = 1.655, df = 1,14, p =

0.101), however, females were assigned to pairs that differed significantly in the size of the test males

(Table 2.3.4), which raises some concerns about females choice being hindered by extremes in male size

forcing a sub-optimal choice. The difference between the mass of the female and the larger male (F =

2.579, df = 1,14, p = 0.008), and also between the mass of the female and the smaller male (F = 3.328, df

= 1, 14, p = 0.001) differed significantly among male pairs.

Interestingly, there was some evidence for a female preference being condition-dependent (Fig.

2.3.6). I calculated the spearman rank correlation between female size and the relative proportion of time

58.

spent with the preferred male for all 15 pairs. The mean correlation was significantly greater than zero

(mean rs = 0.307, n = 15, p = 0.024; one-sample t-test) showing that larger females exhibited a stronger

preference for the preferred male than smaller females. Using the same approach, there was also

evidence of size assortative mating (Fig. 2.3.7). Larger females had a tendency to spend relatively more

time with larger males compared to the time they spent with smaller males (mean rs = 0.253, n = 15, p =

0.072; one-sample t-test).

59.

Table 2.3.1 Wilcoxon Signed Ranks test comparing the mean values across the four females assigned to

each pair for the large and small male (n = 15 male pairs).

Response Variable Mean ± SD Z P-value

Mean of Number of Visits

Large - 9.27 ± 2.95

Small-8 .43 ±3.23 -0.995 0.320

Mean of Total Duration (sec)*

Large - 556.39 ± 224.27

Small-296.45 ± 194.38 -2.101 0.036

Mean of Mean Duration (sec)*

Large - 144.89 ± 138.10

Small - 54.04 ± 52.43 -1.931 0.053

Mean of Duration Proportion

Large - 0.44 ±0.19

Small-0 .27 ±0.19 -1.647 0.100

Mean of Relative Proportion

Large-61.15 ±23.01

Small-38.85 ±23.01 -1.647 0.100

60.

Table 2.3.2 Linear mixed models with female mass and male mass as fixed factors and female identity as

a random factor). Variables marked * are significant at the 0.05 level.

Response Variable Dependent Variable df F Sig.

Number of Visits Male Size 1,58 0.773 0.206

Female Mass 1,58 1.634 0.386

Total Duration Male Size* 1,117 14.216 0.000*

Female Mass 1,117 2.215 0.148

Mean Duration Male Size* 1,117 6.141 0.015*

Female Mass 1,117 0.089 0.766

Duration Proportion Male Size* 1,117 8.451 0.004*

Female Mass 1,117 2.032 0.157

Relative Proportion Male Size* 1,117 11.879 0.001*

Female Mass 1,117 0.000 1.000

61.

Table 2.3.3 Linear mixed models with male pair as a fixed factor and female identity nested within male

pair identity as a random factor.

Response Variable df F Sig.

Number of Visits 14,45 0.599 0.851

Total Duration 14,105 0.168 1.000

Mean Duration 14,105 0.892 0.569

62.

Table 2.3.4 One way ANOVA on female mass, the difference between female mass and the mass of the

larger male (Larger Male Difference), and the difference between female mass and the mass of the

smaller male (Smaller Male Difference) across pairs.

Response Variable df F Sig.

Female Mass 14, 59 1.655 0.101

Larger Male Difference 14, 59 2.579 0.008

Smaller Male Difference 14, 59 3.328 0.001

63.

3.0 ~

2.5 -

2.0 ”

(J

4>3cr4)S_

fa

1.5 -

1.0 -

0.5 -

0 0 -----

-1000 -800 -600 -400 -200 0 200 400 600

Difference in Mean Total Duration

I800 11000

Figure 2.3.1 The means of the difference in total duration (average across four females per male)

between the larger and smaller male in a pair (Wilcoxon Signed Ranks, Z = -2.101, p = 0.036; n = 15 male

pairs). Positive values indicate that females spent more time with the larger male.

64 .

0.5 -

Difference in Mean Duration

Figure 2.3.2 The means of the difference in mean duration (average across four females per male)

between the larger and smaller male in a pair (Wilcoxon Signed Ranks, Z = -1.931, p = 0.053; n = 15 male

pairs). Positive values indicate that females spent more time with the larger male.

65.

600 -

Large Male Small Male

Figure 2.3.3 Mean ± SE of the total duration of time females spent with large and small males (F =

14.216, df = 1, 117, p< 0.001).

6 6 .

0.50-

Large mile Small male

Figure 2.3.4 Mean ± SE for the duration proportion (proportion of total observation time) females spent

with large and small males (F = 8.451, df = 117, p = 0.004).

67.

Figure 2.3.5 Mean ± SE for the proportion of time females spent with large and small males relative to

the amount of time spent with the other male (F = 11.879, df = 1,117, p = 0.001).

68.

- 1.0 - 0.8 - 0.6 - 0.4 - 0.2 0.0 0.2 0.4 0.6 0.8 1.0

Spearmini’s correlation

Figure 2.3.6 Histogram of Spearman’s rank correlations between female size and time spent with the

preferred male in a pair (n = 4 per correlation) showing that larger females spent relatively more time with

preferred males (one-sample t-test, t = 2.52, p = 0.024, n = 15 male pairs).

69.

5 -

4 “

u 33ss< up N

2 -

1 -H 1* '

t f « - -

4 .

> . ' ,

;

•.

I I I■1.0 - 0.8 - 0.6 - 0.4 - 0.2 0.0 0.2 0.4

Sp eann an*s con- elati on

0.6 0.8 1.0

Figure 2.3.7 Histogram of Spearman’s rank correlations between female size and time spent with the

larger male in a pair (n = 4 per correlation) showing that larger females tended to spend more time with

larger males (one-sample t-test, t = 1.95, p = 0.072, n = 15 male pairs).

70.

2.4 Discussion

I found that female Mogurnda mogurnda discriminated between potential mates along a size

gradient. Females spent a greater amount of total time duration and a longer mean duration with larger

males when measured both as a mean across the four females assigned to each pair, and treating each

females as an individual data point. This result was consistent across all pairs, as was female mass. Of

some concern is the fact that some pairs of males differed significantly in size, raising concerns about

female choice being altered by extremes in male size compelling an artificial choice.

Interestingly, I found that larger females exhibited a stronger preference for the preferred male

than smaller females, implying that female choice in this species is condition-dependent. There was also

evidence of size assortative mating with larger females tending to spend more time with larger males

compared to the time they spent with smaller males.

2.4.1. Females preferred larger males

Females display mating preferences for larger males across many taxa (reviewed in Choe and

Crespi 1997) and this study further supports that trend; female M. mogurnda showed a marked preference

for larger males. There are demonstrated benefits to mating with larger males: larger males are more

likely to win fights (e.g., Kotiaho et al. 1997; Hagelin 2002; Lopez et al. 2002; Reichard et al. 2005) and so

provide access to superior resources. For example in fish, larger males are better at obtaining and

guarding spawning sites (Bisazza and Marconato 1988; Lindström 1988). In addition, there is a potential

genetic benefit if traits that increase success during male-male competition are heritable (Cordero and

Eberhard 2003).

Dominant males are mostly likely to be of higher physiological quality. Some performance

measures have shown to positively predict success in male-male competition, and males with higher

energetic reserves are more likely to be successful in male-male interactions in several animal taxa

(Chellappa and Huntingford 1989; Neat et al. 1998). Female choice for larger, more dominant males might

actually be for males in better physiological condition, thereby also selecting for condition-dependence of

male traits (Bonduriansky and Rowe 2005).

Condition-dependence is most commonly discussed in terms of the increased investment by

males into sexually selected traits to attract mates (see Kokko 1998a and the references therein). The

“handicap principle” suggests that only males of high quality and in a good condition can bear the cost of a

71.

sexually selected trait to attract females and so signal their quality through these secondary sexually

characteristics (Zahavi 1975). Signals of condition, however, don’t necessarily need to be through sexually

selected traits, females might directly observe cues instead of relying on correlated traits. Though M.

mogurnda display no secondary sexual characteristics, increased condition could be expressed as higher

courtship rates (Knapp and Warner 1991; Karino 1995) or higher quality parental care. Parental care is

costly (Drent and Daan 1980a; Stanley 2002; Hanssen et al. 2003) and body condition will affect the

quality of parental care an individual can provide (e.g., Linville et al. 1998, Wilson 1998; Kolm 2004;

Candolin 2000; Voltura et al. 2002; Senar et al. 2002; Halupka and Borowiec 2006). Studies have shown

that females sometimes prefer males of high parental quality, rather than basing their choice on male

dominance or size (e.g., sand gobies; Forsgren 1997) although what cues females base this choice on

isn’t always clear (see 2.4.3.”Comparing measures of mating preference”).

2.4.2. Size assortative mating

In this study I not only found that female M. mogurnda generally preferred larger males, I also

found a weak size assortative mating preference. Size-assortative mating appears to be relatively

common across taxa (e.g., Brown 1990; 1993; Arnqvist et al. 1996; Hegde and Krishna 1997; Harari et al.

1999), and has been found in several species of fish e.g., cichlids (Barlow et al. 1990; Budaev et al.

1999), and coral goby Paragobioon echinocephalus (Kuwamura et al. 1993). Again, when mating is costly

the influence of size appears to be particularly important (Hedrick and Dill 1993; Rowe 1994; Grafe 1997;

Watson et al. 1998). For example, larger males can provide females with more food, are better able to

defend territories or resources, and provide protection from conspecifics and predators (Wiegmann and

Baylis 1995; Ptacek and Travis 1997; Savalli and Fox 1998; Watson 1998). The importance of minimising

these costs may lead to assortative mating (Arnqvist et al. 1996; Rowe and Arnqvist 1996). Although there

are numerous examples of size-assortative mating (inferring a role for female as well as male size in

mating) the question of the specific mechanisms by which this arises is still unclear (e.g., mutual mate

choice, mechanical constraints, arrival at breeding sites).

2.4.3. Condition-dependent female choice

I found that as well as size assortative mating behaviour, larger female M. mogurnda showed a

stronger preference for preferred males, indicating that female mating preferences may be condition-

72.

dependent in this species. This is an interesting result because the evidence of condition-dependent

female preference has received a lot of attention but doesn’t have a great deal of empirical support.

The theories around condition-dependent female choice has gained momentum in the literature in

recent years, and was reviewed recently by Cotton et al. (2006b). There is growing evidence of condition-

dependent female mating preferences in fish, e.g., guppies Poecilia reticulata (Lopez 1999; Syriatowicz

and Brooks 2004), three spined sticklebacks Gasterosteus aculeatus (Bakker et al. 1999), upland bullies

Gobiomorphus breviceps (Poulin 1994) and deep-snouted pipefish Syngnathus typhie (Mazzi 2004) as

well as in insects [e.g., black field crickets Teleogryllus commodus (Hunt et al. 2005)], amphibians [e.g.,

African reed frogs Hyperolius marmoratus, (Jennions et al. 1995)], and birds [e.g., black grouse Tetrao

tetrix (Rintämaeki et al. 1998)].

As discussed, expressing mating preferences exacerbates the costs of mating and logically

females in better condition should be better able to bear these costs than females in worse condition

(Cotton et al. 2006). Alternately, higher quality females may be more discriminating for the same cost than

poorer quality females. As preferences are predicted to be weaker when the costs are higher, the strength

of female preference is expected to vary with female condition by much the same argument that sexually

secondary traits vary with male condition (Pomiankowski 1987; Grafen 1990; Iwasa et al. 1991; Iwasa and

Pomiankowski 1999). For example, Mazzi (2004) showed that experimental infection of both sexes of

deep-snouted pipefish Syngnathus typhie revealed changes in mating preference. Deep-snouted pipefish

are sex-role reversed and males are the choosier sex, so males in good condition showed a strong

preference for uninfected females whereas infected males in worse condition did not discriminate between

infected and not infected females. As such, the first prediction of a system that displays condition-

dependent female choice is that better quality females will showed stronger preferences. This study

satisfied this prediction as larger female M. mogurnda showing stronger preference for the preferred male

in each pair.

Another prediction of condition-dependent choice is size assortative mating (Cotton et al. 2006).

Better quality females should be able to exhibit stronger preferences for the same costs and therefore

have better mates. This may be through more intense searching, or having a higher rejection rate than

lower quality females. This study also satisfied this prediction, with larger female M. mogurnda preferring

larger (higher quality) males than smaller females. Again, using deep-snouted pipefish as an example

species, there is evidence of mutual mate choice with both sexes showing preference for larger partners

(Mazzi 2004). Male condition-dependent preference was particularly sensitive to female infection status

73.

amongst small females who have lower than average fecundity, suggesting that one of the main factors

underlying male preference is the selection of mates in order to increase the number and quality of eggs

received. The influence of size on parental care behaviours in M. mogurnda will be discussed in Chapter

3.

The final prediction is that females of higher genetic quality should also show stronger mating

preferences for better quality males than females with lower genetic quality. This is because females with

high genetic quality will do better in any given environment than females of lower genetic quality and

therefore the mechanisms of condition-dependent choice should be the same across different

environments, i.e. mating decisions should be maintained. The scope of my study did not cover the

genetic quality of my fish across environments but this would be a clear avenue for a subsequent study.

2.4.4. Comparing measures of mating preference

Having argued that females demonstrated mating preferences for larger males across many taxa

(reviewed in Choe and Crespi 1997) and appear to do so in this study, the assumption that females prefer

larger, presumably more dominant, males has been challenged on numerous occasions (Qvarnstrom and

Forsgren 1998). Dominant males may impose direct (e.g., Leboeuf and Mesnick 1991; Preston et al.

2001; Wong 2004) and indirect (e.g., Chippindale et al. 2001) costs on females, making them less

attractive as mates.

As discussed, traditional mate choice tests by means of simultaneous choice tests have their

problems. Even in studies like this one, where the effect of male-male competition has been controlled for,

and physical and chemical contact between the female and males has been maximised, female mate

choice is still being indirectly measured and this indirect measure is only assumed to equate to actual

mating success. Another way to measure male attractiveness is to conduct no-choice tests (e.g., Pilastro

et al. 2002; Shackleton et al. 2005) that measure latency to mating. Measuring attractiveness as mating

latency has several benefits: females are allowed to base their choice on the entire suite of physical and

chemical cues males offer; and female mating preference can be determined from an actual mating. In

Chapter 3, I discuss how I used the days until spawning as alternate measure of mating preference and

compare it to the results from this chapter.

74.

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CHAPTER 3 Spawning and parental care in the

northern trout gudgeon (

mogurnda)

3.1 Introduction

Parental investment theories predict that selection favours individuals that maximise their lifetime

reproductive success. There are both costs and benefits to each reproductive event and therefore a trade­

off between present and future reproduction (Williams 1966b; Trivers 1972; Gross and Sargent 1985;

Sargent and Gross 1985; Clutton-Brock 1991). The costs of parental care include expenditure of energy

and time, and loss of foraging and mating opportunities (Clutton-Brock 1991; Balshine-Earn 1995; Smith

and Wootton 1995; Mackereth et al. 1999), and the investment in parental care is beneficial by increasing

the current reproductive success of parents (Sargent and Gebier 1980; Zoran and Ward 1983; Kunzler

and Bakker 2000; Karino and Arai 2006). In species with male parental care, it has been suggested that

females pay attention to the willingness of their future mate to invest in offspring and the quality of the

care they will provide (Möller and Thornhill 1998).

3.1.1. How much to invest in parental care: balancing costs and benefits

Parents have to make decisions on how much to invest in each clutch and how to adjust their

expenditure in response to variation in costs and benefits (Winkler 1987). Finding the optimal trade-off of

costs and benefits to maximise net fitness is complex. For example, an increased risk of predation

increases the benefits of caring for young but also increases the potential costs to the parent thereby

resulting in a reduction in future reproductive success. Lindström (1998) found that male sand gobies

Pomatoschistus minutus only continued to guard eggs in the presence of a predator (which increased the

cost of care) when the clutch was large (when the benefit was higher). This suggests that males only

continue caring for eggs if the benefit of investing in the current clutch outweighs the cost to future

reproductive success.

If the costs become too great, parents can decide to abandon the reproductive event completely.

Filial cannibalism and desertion is commonly reported in fish with male parental care (Rohwer 1978;

Petersen 1990; FitzGerald 1992b; Marconato et al. 1993; Okuda and Yanagisawa 1996; Lindström and

8 8 .

Sargent 1997; Lindström 1998; Jennions and Polakow 2001; Manica 2002b; Payne et al. 2002). Females

have, however, developed a strategy to help reduce this loss. Males usually only fully cannibalise clutches

that are small (Sargent 1992) and females have been shown to increase the clutch size of males by

preferentially spawning with those who are already guarding eggs (Marconato and Bisazza 1986; Unger

and Sargent 1988; Petersen 1990; Kraak and Groothuis 1994; Forsgren et al. 1996; Goulet 1998;

Reynolds and Jones 1999). The cost of even partial filial cannibalism will be diluted if a male is guarding

several clutches of eggs (Forsgren et al. 1996).

Other factors that affect the amount of parental investment in care include the reproductive value

of the parents, the age of the offspring and the physical condition of the parents (Trivers 1985; Sargent

1997; Takegaki and Nakazono 1999; Lissaker et al. 2003; Manica 2003; Pampoulie et al. 2004).

Investment in care is also affected by factors such as environmental gradients (Schaffer 1974a; Kramer

1987; St Mary et al. 2001; Hale et al. 2003) and clutch size (Karino and Arai 2006). Parental care

behaviours are discussed in detail in Section 3.1.7 (“Variation in parental care behaviours”).

3.1.2. Paternal care in fish

Although in many taxa female-only care is the predominant form of care (Clutton-Brock 1991), the

majority of fish display male parental care (Gross and Sargent 1985). The majority of external fertilisers

(76%) display male parental care, which usually involves defence of a territory by more than one female

(Gross and Sargent 1985). Mank et al. (2005) showed that paternal care was by far the most common

form of care in ovuliparous fish (41 families) compared to five incidences each for maternal and biparental

care. Individuals control their own level of care and, aside from mammalian offspring that require nutrition

from the mother in the form of lactation, either parent can provide the necessary care in most breeding

systems. Sole parental care by the male seems counter-intuitive, however, in the light of the costs

discussed in Chapter 1. So how is it so feasible?

Mank et al. (2005) showed that paternal care appears to have evolved straight from the

generalised basal condition of external fertilisation at least 22 times. They also showed that Actinopterygii

display phenotypic expressions of sexual selection, most commonly sexual dichromatism (Reimchen

1989; Houde and Endler 1990; Stott and Poulin 1996; Amundsen and Forsgren 2001). Sexual

dichromatism was positively correlated with paternal care, which suggests that the competition for mates

that drives sexual selection also drives the evolution of parental care. Furthermore, nest construction was

also positively correlated to paternal care, and generally preceded it. Parental care may have grown from

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the territorial defence of spawning sites by males: nest construction may be a pre-adaptation for male

parental care.

Several reasons have been put forward to explain why paternal care is so common in external

fertilisers. Firstly, males have higher confidence in paternity with external fertilisation (Trivers 1972)

therefore males are more likely to invest care in eggs as the mean benefits are higher (Neff and Gross

2001). Secondly, based on the assumption that females release gametes first, this favours female

desertion leaving the male to either care for the eggs or desert (Trivers 1972; Dawkins and Carlisle 1976).

Finally, even if the benefits of care are equal for both sexes, the costs to males are lower as they can

guard clutches from several females simultaneously with a reduced loss in mating opportunities (Blumer

1979). Males with eggs already in their nests are actually preferred by females in some species further

reinforcing the evolution of paternal care (Unger and Sargent 1988; Kraak and Groothuis 1994; Forsgren

et al. 1996; Goulet 1998; Reynolds and Jones 1999).

When one parent (male or female) can successfully be the sole provider of care, this presents the

opportunity for their mates to manipulate the relative contributions of parental investment. The benefits of

manipulating a partner’s expenditure on care results from sexual conflict between the sexes.

3.1.3. Sexual conflict over parental care

Conflict exists because the costs of parental care are usually disproportionately carried between

individuals but the benefits are shared equally (Trivers 1972; Parker et al. 2002). Therefore, a parent who

manipulates the other parent into increasing his or her investment into the current reproductive event will

enjoy a selective advantage.

Early studies argued that males are more likely to benefit from investing less care as they have

greater potential reproductive rates (Clutton-Brock 1991). Males gain more from investing effort into

gaining additional matings than providing care, and this is the basis of the traditional argument as to why

parental care is predominantly provided by females in most taxa (Bateman 1948; Trivers 1972). As

discussed in Chapter 1, however, every offspring has one mother and one father and the average

reproductive rates are equal between the sexes. Queller (1997) remedies this flaw in the argument by

noting that if a subset of “attractive” males are gaining the majority of matings then the reproductive rate of

the average male is irrelevant because the ‘average’ male does not mate. The reproductive rate of mating

males is higher than that of females and the decision to expend energy seeking new mates rather than

providing care is beneficial and provides an evolutionary stable strategy for males.

90.

This asymmetry provides a feasible model for why females tend to provide more care than males,

particularly as sexual selection (and male-male competition) intensifies (Clutton-Brock and Parker 1992).

When females provide more care, this creates a positive feedback loop if fewer and fewer males can

monopolize an even greater share of the available females due to greater female choosiness or male-

male competition having a stronger effect on determining which males gain access to mates.

3.1.4. Adjusting parental investment: responding to partner effort

Experimental studies suggest that the amount of care each parent provides is likely to be a

responsive dynamic process of negotiation rather than a predetermined decision (Dawkins and Carlisle

1976; Webb et al. 1999; McNamara et al. 2000). Recent studies actually suggest that parents may benefit

from handicapping themselves and thus manipulating their mate to compensate for their decreased efforts

(Marques 2004; Osorno and Szekely 2004; Houston et al. 2005). There is evidence to show that when

one mate decreases their effort in care, the partner will increase their efforts in compensation. For

example, in the starling Sturnus vulgaris when the parental effort of one parent is experimentally

decreased, the other mate responded by increasing their level of care (Wright and Cuthill 1989).

Studies that looked at the amount of compensation a parent provides have, however, produced

varied results. By clipping feathers or attaching small weights, bird researchers can increase the costs of

care and manipulate the parental effort of a mate (measured by feeding rate). These studies aim to

measure the corresponding change in effort of the other partner, which ranged from no difference

(Whittingham et al. 1994; Sanz et al. 2000), to both an increase (Slagsvold and Lifjeld 1988) and a

decrease (Markman et al. 1995) in effort. Whittingham et al. (1994) handicapped both male and female

great tits Parus major, and found no overall effect on the combined feeding rate of pairs but the responses

from birds were complex. The sexes differed in their response, with handicapped males decreasing their

feeding rates while handicapped females did not. In response, females partnered with a handicapped

male fully compensated for their decrease in work rate, but males mated with a handicapped female did

not show any compensation and even tended to decrease their feeding rates (Whittingham et al. 1994).

Theory predicts that compensation should only be partial, not full, otherwise a parent could

decrease it’s own effort without reducing the total effort to the offspring which is clearly an unstable

evolutionary strategy (Houston et al. 2005). Contrary to this, however, Osorno and Szekely (2004) showed

near full compensatory parental effort after a male has deserted the nest in magnificent frigatebird Fregata

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magnificens. In this case, rather than responding to the relative effort of a mate, females might instead

respond to the condition of their mates (Schwagmeyer et al. 2002).

3.1.5. Adjusting parental investment: responding to partner condition

Logically, an individual should choose a mate in good condition to provide better care for their

offspring. The good parent hypothesis predicts that secondary sexual characteristics should signal an

individual’s ability to provide care (Heywood 1989; Hoelzer 1989), but studies provide evidence that both

support (Linville et al. 1998; Buchanan and Catchpole 2000; Soler et al. 2001) and contradict (Smiseth

and Amundsen 2000; Smiseth et al. 2001) this prediction. As discussed in Chapter 1, sexually selected

traits are expensive to produce (Kotiaho 2001) and often demonstrate a trade-off with other life history

traits (Hunt et al. 2004). So it may be that males with more attractive traits are in fact not in better

condition (Grafen 1990; Kokko 2001; Hunt et al. 2004; Tomkins et al. 2004), or do not honestly signal their

condition (Candolin 1999b).

Kokko (1998b) provides a model of parental care and attractiveness in which males allocate

energy expenditure to self-maintenance, sexual advertising and parental care to maximise their fitness. If

there are diminishing returns from advertising and care (i.e. reduced benefits to extra matings or reduced

opportunities for extra matings), advertising will be an honest indicator of male care and females will prefer

these males. This model, however, doesn’t predict how much a female will allocate to a reproductive event

due to the attractiveness of the male or the effect of indirect genetic benefits and adding these factors into

the model could change the conclusions (Houston et al. 2005).

As previously mentioned, attractive males may decrease their parental care effort because they

gain more from investing in seeking new mates due to their higher reproductive rate. Females mated to

theses attractive males, however, may increase their effort by allocating a greater investment into those

reproductive events (Cunningham and Russell 2000). Known as the ‘differential allocation hypothesis’

(Burley 1988; Sheldon 2000), females may increase expenditure on offspring because the offspring are

more valuable (Sheldon 2000) or as an attempt to retain their attractive mate (Burley 1988).

The question of what cues females use for mate choice and the honesty of these cues relating to

condition and parental care can be less obvious in species where males do not display secondary sexual

ornaments. In fish, females have been shown to use parental care as an outright cue for mating

preferences, preferring males that exhibit parental care to a greater degree and have a higher associated

hatching success (Downhower and Brown 1980; Unger and Sargent 1988; Knapp and Kovach 1991;

92.

Forsgren et al. 1996; Forsgren 1997). Studies have reported females preferring quality of parental care

over more traditionally traits such as dominance (e.g. pacific blue-eye fish, Wong 2004). In situations

where the trait used for mate attraction is (or is correlated to) male care quality, it is expected to be under

sexual selection (Kirkpatrick 1985). This creates an interesting dynamic in which the traditional trade-off

between current and future reproductive success is lessened because there is less trade-off between

parental care (current reproduction) and expressing traits under sexual selection (future reproduction).

Care might even be used as a courtship display and so increased in the presence of receptive females

(Fitzpatrick et al. 1995; Kokko 1998b).

3.1.6. Parental care and mate choice

Parental care: correlated traits

In fish, there is a wide literature showing females prefer larger males in species that show

biparental or paternal care (Downhower and Brown 1980; Noonan 1983; Keenleyside et al. 1985; Goto

1987; Bisazza and Marconato 1988; Cote and Hunte 1989; Rogers and Barlow 1991). Larger and more

dominant males are more likely to be of higher physiological quality (e.g., Chellappa and Huntingford

1989; Guderley and Couture 2005) and female mate choice for larger males might mask a preference for

better physiological condition, thereby also selecting for condition-dependence of male traits

(Bonduriansky and Rowe 2005).

The condition of a male or his quality in terms of parental care is often related to his size. For

example, guarding is one of the most common forms of parental care in fish and there appears to be a

large male advantage in nest defence. Larger males are better at acquiring and guarding spawning sites

(Bisazza and Marconato 1988; Lindström 1988) and their ability to obtain better quality nesting sites could

also contribute to an increased survival rate of eggs (Hastings 1988; Cote and Hunte 1989; Kvarnemo et

al. 1998). Guarding is a foraging limiting activity (Kraak and Videler 1991; Kraak 1996; Payne et al. 2002),

and males have been shown to lose weight by the end of the caring period (Coleman and Fischer 1991;

Maekawa et al. 1996; Jones and Reynolds 1999; Skolbekken and Utne-Palm 2001) which selects for

males that are initially in better condition. Where dominance does not equate to increased parental care,

however, females often choose overall paternal quality over male fighting ability (Forsgren 1997; Wong

2004; Wong and Candolin 2005).

93.

Other factors effecting female choice - filial cannibalism

Females also choose mates based on other male traits such as courtship (Knapp and Warner

1991; Östlund and Ahnesjö 1998), nest characteristics (Sargent and Gebier 1980), and number of eggs in

a nest. The incidence of females preferentially choosing to lay their eggs with males who already have

eggs in their nest is widespread (Marconato and Bisazza 1986; Unger and Sargent 1988; Cote and Hunte

1989; Petersen 1990; Kraak and Groothuis 1994; Forsgren et al. 1996; Goulet 1998; Reynolds and Jones

1999; Jennions and Polakow 2001; Okuda et al. 2002). There may be several reasons for this: (1) to

reduce the risk of males eating the whole clutch or abandoning the nest by increasing total clutch size

(Rohwer 1978); (2) to reduce the proportion of her eggs that are eaten during care (e.g., Forsgren et al.

1996); (3) to increase male parental investment by increasing clutch size (e.g., Coleman et al. 1985;

Karino and Arai 2006); and (4) to increase the chance that a male is a high quality parent (mate choice

copying) (Kraak and Videler 1991).

If the costs of care are too great (or the benefits too small), males often eat their own eggs (filial

cannibalism) or desert the brood to regain condition to invest in future reproduction (FitzGerald 1992b;

Marconato et al. 1993; Kraak 1996; Okuda and Yanagisawa 1996; Kvarnemo et al. 1998; Marques 2003).

This behaviour is adaptive for males, who benefit in terms of resource consumption but represents a loss

of investment for the female. Expenditure on small clutches presents a low return on investment which

may be better allocated to future broods, so whole clutch filial cannibalism is usually found when males

have small or low quality clutches (Petersen 1990; Sargent 1992; Smith 1992; Svensson et al. 1998;

Manica 2002a; Lissaker et al. 2003; Manica 2003; Karino and Arai 2006). Experimental reductions of

clutches have shown that parents have a threshold below which a clutch is totally cannibalised (Lavery

and Keenleyside 1990) or a male will abandon his eggs (Jennions and Polakow 2001). Females who

preferentially lay eggs in nests where there are already eggs present will increase the clutch size of a

male’s brood and therefore decrease the likelihood of losing her investment to whole clutch filial

cannibalism or desertion.

Males do not always eat the entire clutch; sometimes they eat only a portion of their eggs. Partial

clutch cannibalism is theorised to be a method of regaining energy lost from care to invest into current or

future offspring (Unger and Sargent 1988; Forsgren et al. 1996; Reynolds and Jones 1999). The

behaviour is therefore adaptive as it can reduce the loss of condition and increase a male’s overall

reproductive success by increasing the hatching success of the current reproductive event and

maintaining condition for future clutches (Sargent 1985; Smith and Wootton 1995). As with whole clutch/or

94.

cannibalism, females who choose to lay eggs in nests where there are already eggs present will dilute the

effect of partial cannibalism on her eggs by increasing the total clutch size.

Evidence that males devote greater amounts of parental investment into larger clutches is

widespread in fish (Coleman et al. 1985; Sargent 1988; Forsgren et al. 1996; Karino 1997; Jennions and

Polakow 2001; Suk and Choe 2002; Manica 2003; Karino and Arai 2006) though some studies have found

no relationship between clutch size and effort (Knapp and Warner 1991; Skolbekken and Utne-Palm

2001). Females who preferentially lay their eggs to maximise their mates clutch size should be at a

selective advantage and receive direct benefits for this behaviour. Finally, it has been suggested that a

female preference for males with large broods might be adaptive because the number of eggs present in

the nest is probably a reliable predictor of the survival chances of the eggs (Kraak and Videler 1991).

Overall parental investment is also affected by the environmental conditions, such as temperature

(Skolbekken and Utne-Palm 2001; Cooke et al. 2003) and oxygen level (Lissaker et al. 2003).

3.1.7. Variation in parental care behaviours

Fanning

Variation in specific parental care behaviours are also affected by the costs and benefits of caring.

Fanning behaviour is a very common form of care in fish (Blumer 1979) and entails oxygenation of the

embryos by fanning the eggs with the fish’s pectoral fins. Fanning is often the most important factor in

hatching success (Sargent 1988; Kraak 1996; Lindström 1998; Karino and Arai 2006) and egg

development rate (e.g., Sargent and Gebier 1980; Zoran and Ward 1983; Karino and Arai 2006). Fanning

increases water circulation and gas exchange (Wootton 1998; Green and McCormick 2005), which is

important as reduced oxygen availability retards embryo development and increases mortality (Kunzler

and Bakker 2000). When oxygen levels are low, an increase in ventilation of nests by fanning more water

over the eggs has been noted in many species of fish, e.g., sticklebacks Gasterosteus aculeatus (van

lersel 1953; Reebs et al. 1984) and gobies (Torricelli et al. 1985; Jones and Reynolds 1999; Skolbekken

and Utne-Palm 2001). Fanning is also effected by changes in temperature and salinity (St Mary et al.

2001) and clutch size (Karino and Arai 2006).

Filial cannibalism

As discussed, filial cannibalism has been widely recorded in fish (recorded in 17 families, Manica

2002) , and across other taxa (Polis 1981). Partial clutch cannibalism as a means for males to recuperate

95 .

lost condition and energy assumes that caring males are food limited, and many findings support this

claim (Sargent 1985; Itzkowitz and Makie 1986; Demartini 1987; Hoelzer 1992; Sargent et al. 1995; Smith

and Wootton 1995). Payne et al. (2002), found that males fed a supplementary diet gained more weight

than control males but interestingly, that did not equate into an increase in hatching success. Loss of

condition does appear to affect the filial cannibalism though, Kvarnemo (1998) for example found that

males whose diets where supplemented decreased their rate of filial cannibalism but did not erase it all

together. On the other hand, other studies have found no clear relationship between nutritional status and

filial cannibalism (Belles-lsles and Fitzgerald 1991; Kvarnemo 1997; Lindström and Sargent 1997;

Vinyoles et al. 1999).

Payne et al. (2002) propose an alternate theory for filial cannibalism: increasing available oxygen

to the eggs. Reducing egg density increased development time and hatching success, probably as a

function of increasing oxygen availability to the embryos. Males in lowered dissolved oxygen (DO) levels

consumed relatively more eggs consistent with this explanation. An alternative possibility, however, is that

this could simply be a function of fact the energetic costs of care are increased under low DO (Kamler

1992). A oxygen mediated model showed that males who cannibalise a high fixed proportion of their eggs

had higher hatching success than males who cannibalised a low proportion or none at all (Payne et al.

2004).

Another proposed reason for partial filial cannibalism is control of disease or infection. Males may

not be eating healthy eggs, they may instead be cannibalising dead, unfertilised of diseased eggs

(Hoelzer 1988; Kraak 1996). Though Kraak (1996) showed males selectively ate dead eggs, the rate of

filial cannibalism is mostly well above the natural rate of diseased eggs so this can only offer a partial

explanation for egg predation (Kraak 1996; Klug et al. 2005). It has also been proposed that eggs provide

a source of particular nutrients important to the male (Belles-lsles and Fitzgerald 1991; Sargent 1992) but

experimental evidence shows males fed with other male’s embryos (eggs from another male’s nest) do

not have a lower incidence of cannibalism on their own clutch (Kvarnemo et al. 1998).

96.

3 .1.8 . Aims of this study

In this experiment, I aimed to quantify and record the parental care behaviours of Mogurnda

mogurnda, which as far as I am aware, has not been documented before. For each male, I measured

variables such as spawning time, egg fanning, egg guarding, filial cannibalism, desertion and fanning rate.

Relating these variables back to my results from Chapter 2, I wanted to determine if:

(a) there are honest (i.e. predictable) cues to male parental care quality;

(b) these are the same characters used by females to make their mating preferences; and

(c) male preference shown in Chapter 2 from association preference tests is congruent to the

results in this chapter where I used latency to mating as an alternative measure of female preference for a

male.

97.

3.2 Methods

As described for the mate choice trials (Chapter 2) all aquaria were kept at 26° Celsius in climate-

controlled rooms, and on a 14:10 hr day: night illumination cycle. Holding tanks (6’ x 2’ x 2’) where fish

were kept between experiments were connected to sump filters filled with bioballs containing bacteria that

break down waste products in the water. Four holding tanks were used, two for fish before experiments

and two for after experiments while keeping the sexes separate.

3.2.1. Parental Care

Having selected pairs of males that differ significantly in attractiveness (Chapter 2), I randomly

assigned two similarly sized breeding females to each male pair. Each male was then put into a separate

breeding tank with one female. All breeding tanks (36” x 18” x 18”) had adequate filtration and I kept water

quality high with weekly 25% water changes. Each tank had three spawning sites comprising two white

rectangular tiles at opposite ends and a piece of plastic piping.

I checked every tank for spawning every 1-2 days and I recorded each time that a pair spawned

(or if they had failed to do so after 60 days). I also recorded male parental care behaviour using

JWatcher™ (Blumstein et al. 2000) until the eggs hatched or were eaten. I recorded male behaviour for 10

minutes per recording session, with 1-2 days between sessions. The behaviours I recorded included the

frequency and duration of fanning bouts, the intervals between fanning bouts, fin beat rate (average

number of fin beats per second), time spent guarding (resting on top of the eggs), time guarding (near the

eggs), time away from the eggs and any observations of filial cannibalism. I then analysed the parental

care behaviour data to test whether there was any effect of male size or male “attractiveness” on the

various measures of parental quality.

3.2.2. Statistical Analyses - Parental Care Analysis

To analyse whether mate choice preference inferred from latency to mating (no-choice tests) was

congruent with the preferences seen in the traditional association mate choice tests, I used survival

analyses (Kaplan Meier) to compare the number of days until the first spawning occurred between large

and small males, as well as between preferred and non-preferred males (i.e. survival is equivalent to how

long it was until a male’s status changed from no spawning to spawning). The data was right censored if

the male had still not spawned at the end of the study period (60 days).

98 .

In the parental care behaviour analyses, I analysed sources of variation in the following parental

care behaviours that were recorded during the mating experiments:

• Attack was when a male left the eggs to chase away another fish.

• Away was when a male left the eggs for another reason.

• Fanning was when a male used his pectoral fins to fan the eggs to facilitate the flow of fresh

oxygenated water over them.

• Flare was when a male flared his operculum at another fish in warning.

• Near was when a male was within 10cm of the eggs but not directly over them.

• Rest was when a male was lying directly over the eggs but was not fanning them.

• Fan beat rate was the average number of fanning beats per second.

I first calculated the mean value by pooling across all observations for a given male. I then

compared individual means between large and small males, as well as between preferred and non­

preferred males, for each variable using Mann-Whitney U tests. I did not used paired statistical tests (i.e.

pairing by male test pair) as there were too few cases where data was available from both males. I also

compared the proportion of spawning attempts in which filial cannibalism occurred between males that

differed in size class (large or small), as well as the number of spawning attempts because this could be

another measure of male attractiveness since it stands to reason females would more readily remate with

an attractive male. Finally, 1 used linear mixed models to analyse variation in hatching time while

controlling for the fact that some males had multiple clutches and treated male identity and pair identity as

random factors.

99 .

3.3 Results

I found no effect of male size or male attractiveness on guarding or fanning behaviours in

Mogurnda mogurnda. There was no difference in the number of occurrences, the total duration or the

mean duration of a bout between large and small males for guarding or fanning behaviours (Table 3.3.1

and Table 3.3.2). There was also no significant difference in these parental care behaviours between

males that differed in attractiveness (Table 3.3.3 and Table 3.3.4). Disappointingly, there was no effect of

male size class (Mann-Whitney U = 105.500, Z = -0.392, p = 0.775) or attractiveness (Mann-Whitney U =

88.500, Z = -1.343, p = 0.325) on the proportion of clutches where filial cannibalism occurred. There were,

however, only eight incidences of filial cannibalism from seven of the 30 males, with only 13% of all

spawning attempts (8 out of 61) showing any incidences of filial cannibalism and they were all whole

clutch cannibalisms. Small samples sizes may have contributed to these non-significant results for these

behaviours as not all males performed all behaviours (see tables for sample sizes).

Unexpectedly, I found that preferred males had significantly lower fanning rate than non-preferred

males (Mann-Whitney U = 43.00, Z = -2.892, p = 0.004, Fig. 3.3.1). Non-preferred males had an average

fanning rate of 1.21 beats per second, and preferred males having a mean fanning rate of 0.73. There

was no effect of male size class on fanning rate (Mann-Whitney U = 94.00, Z = -0.770, p = 0.461).

There was no effect of male size on time to spawning (Fig. 3.3.2; Kaplan Meier, Chi-square =

0.064, df = 1, p = 0.801). Contrary to expectation however, preferred males actually took significantly

longer to spawn than non-preferred males (Kaplan Meier, Chi-square = 5.396, df = 1, p = 0.020;

Fig. 3.3.3). Preferred males spawned after an average of 27.1 days, while non-preferred males took an

average of 7.9 days. Closer analysis of the data, however, showed that five preferred males did not spawn

at all which could explain the result. Interestingly, three of the five males who did not spawn were from

pairs where the smaller male was preferred over the larger male.

There was no difference in the total number of spawning attempts per male between males that

differed in attractiveness (Mann-Whitney U = 86.00, Z = -1.120, p = 0.285) or in size (Mann-Whitney U =

107.00, Z = - 0.232, p = 0.838). Finally, there was no effect of male mass (treated as a continuous

variable) (F = 81.802, df = 58, p = 0.544) or attractiveness (F = 81.026, df = 58, p = 0.570) on the number

of days until eggs hatched.

100.

Table 3.3.1 Comparison of the number of occurrences in the 10 minute observation period for each

parental care behaviour between large (n = 13) and small (n = 12) males (Mann-Whitney test).

Parental Care Behaviour Mean ± SD Mann-Whitney U Z Sig.

Attack

Large - 0.00 ± 0.00

Small - 0.00 ± 0.00 78.00 0.000 1.000

Away

Large - 2.15 ± 2.99

Small-2 .17 ±2.79 72.00 -0.338 0.735

Fanning

Large - 15.68 ± 9.93

Small - 10.85 ±8.77 58.00 -1.090 0.276

Flare

Large - 0.00 ± 0.00

Small - 0.00 ± 0.00 78.00 0.000 1.000

Near

Large - 6.19 ± 6.622

Small-5 .17 ±3.633 77.00 -0.055 0.956

Rest

Large — 6.96 ± 6.02

Small-7 .54 ±5.89 71.00 -0.381 0.703

101.

Table 3.3.2 Comparison of the total and mean durations of time (seconds) spent in the 10 minute

observation period engaged in parental care behaviours between large and small males (Mann-Whitney

test).

Variable Behaviour Mean ± SD Mann- Whitney U Z Sig.

Total Away Large - 137.21 ± 205.79 (n=7)

Duration(sec) Small - 137.52 ± 171.31 (n=8) 26.00 -0.231 0.817

Fanning Large - 208.66 ± 177.21 (n=9)

Small - 212.27 ± 199.61 (n=11) 75.50 -0.136 0.892

Near Large - 153.95 ± 107.37 (n=9)

Small - 165.72 ± 134.93 (n=11) 46.00 -0.266 0.790

Rest Large - 197.25 ± 203.08 (n=12)

Small - 122.31 ±87.45 (n=11) 60.00 -0.369 0.712

Mean Away Large - 98.09 ± 220.93 (n=7)

Duration(sec) Small-34.24 ±29.16 (n=8) 21.00 -0.810 0.418

Fanning Large - 19.75 ± 16.55 (n=9)

S m a ll-28.69 ± 24.19 (n=11) 62.50 -0.843 0.399

Near Large - 28.74 ± 28.22 (n=9)

Small - 33.77 ± 35.27 (n=11) 48.00 -0.114 0.909

Rest Large - 49.44 ± 88.44 (n=12)

Small - 17.53 ± 15.20 (n=11) 52.00 -0.862 0.389

102.

Table 3.3.3 Comparison of the number of occurrences in the 10 minute observation period for each

parental care behaviour between preferred (n = 13) and non-preferred (n = 12) males (Mann-Whitney

test).

Parental Care Behaviour Mean ± SD Mann-Whitney U Z Sig.

Attack

Pref - 0.00 ± 0.00

Non-pref - 0.00 ± 0.00 75.00 0.000 1.000

Away

Pref - 2.05 ± 2.62

Non-pref - 2.23 ± 3.06 72.00 -0.172 0.863

Fanning

Pref-12.67 ±9.08

Non-pref - 14.07 ± 10.53 73.00 -0.111 0.912

Flare

Pref - 0.00 ± 0.00

Non-pref - 0.00 ± 0.00 75.00 0.000 1.000

Near

Pref - 6.90 ± 5.98

Non-pref - 4.90 ± 4.87 59.00 -0.892 0.372

Rest

Pref-5 .65 ±4.76

Non-pref - 8.30 ± 6.39 57.50 -0.972 0.331

103.

Table 3.3.4 Comparison of the total and mean durations of time (seconds) spent engaged in parental

care behaviours between preferred and non-preferred males (Mann-Whitney test).

Variable Behaviour Mean ± SD Mann- Whitney U Z Sig.

TotalDuration(sec)

Away

P re f- 123.12 ±210.67 (n=7)

Non-pref- 149.85 ± 164.99 (n=8) 21.00 -0.810 0.418

Fanning

Pref-223.20 ±191.60 (n=7)

Non-pref - 190.60 ± 182.85 (n=8) 60.50 -0.804 0.421

Near

Pref - 191.12 ±117.00 (n=8)

Non-pref - 139.96 ± 123.06 (n=12) 36.00 -0.926 0.355

Rest

Pref - 162.23 ± 169.08 (n=9)

N on-pref-160.88 ± 160.21 (n=14) 61.00 -0.126 0.900

MeanDuration(sec)

Away

Pref-98.70 ±210.67 (n=7)

Non-pref - 33.70 ± 29.52 (n=8) 24.00 -0.463 0.643

Fanning

Pref-27.37 ±23.69 (n=7)

Non-pref - 19.48 ± 15.47 (n=8) 56.50 -1.026 0.305

Near

Pref - 34.40 ± 30.94 (n=8)

Non-pref - 29.58 ± 33.20 (n=12) 41.00 -0.540 0.589

Rest

Pref-30.28 ±33.81 (n=9)

Non-pref - 36.69 ± 80.78 (n=14) 57.00 -0.378 0.705

104.

10-

~a

Non-Preferred Male Preferred Male

Female Preference

Figure 3.3.1 Mean ± SE for the fanning rate of non-preferred and preferred males.

105 .

1 0 «

Days To Spawn

Figure 3.3.2 Kaplan Meyer survival graph showing the number of days before males first spawned. Data

for males that did not spawn after 30 days was right censored. Contrary to expectation, non-preferred

males (bottom) spawned sooner that preferred males (top line) (Kaplan-Meier survival analysis, Mantel-

Cox = 5.396, p = 0.020, n = 30).

106.

40 -

30 -

c

Non-preferred Male Preferred Male

Figure 3.3.3 Mean ± SE for number of days before spawning for non-preferred and preferred males.

107.

3.4 Discussion

3.4.1. Variation in parental care quality

In this chapter, I first aimed to see if there were any honest (i.e. predictable) cues to male parental

care quality. Interestingly, I did not find any effect of male size on any parental care behaviours, so size

was not a predictor of parental quality. There was no effect of male size on guarding, fanning, filial

cannibalism or egg development time. This suggests that male size (and by association, male dominance)

does not correlate with parental quality.

If there were any cues to male parental care quality, I wanted to compare them to the characters

used by females to select mates in Chapter 2. Male size per se does not predict care, but if we assume

that male attractiveness is correlated to one or more traits that females base their choice on, male

attractiveness could be treated conceptually as a trait when looking for effects on care behaviour. The

non-significant response for all parental care behaviours is repeated for males differing in attractiveness,

except in the case of fanning rate. Unexpectedly, preferred males fanned at a lower rate. This poses a

dilemma as it makes female choice maladaptive, with females actually suffering a cost of decreased male

care from their mating preference. This leads to the question of how female choice is maintained in this

species if females are incurring higher costs for their mating preferences. There are several possible

explanations for the discovery of maladaptive female choice in this study; females could be gaining

material benefits unrelated to parental care or females could be gaining genetic benefits. Another

explanation is that my method for discriminating female preference is not accurate which I discuss later.

Maladaptive female choice

Mogurnda mogurnda joins the list of species in which attractive or more actively courting males

provide less care (Burley 1988; de Lope and Möller 1993; Burley et al. 1996; Qvarnström 1997; Raouf et

al. 1997; Griffth et al. 1998) a prediction generated by the model of differential allocation (Burley 1986). It

is unclear what impact this cost would have on actual reproductive success as I wasn’t able to measure

hatching success. The eggs were too small to count from a distance of 20 cm and males were very

sensitive to predation risk while guarding a clutch and would abandon the eggs if I disturbed them. I had to

be very careful even moving the front cover slightly to observe parental care behaviours, and males

frequently abandoned their eggs during my pilot study until I learned what level of disturbance they would

tolerate. It is difficult to draw quantative conclusions about the cost of this choice but fanning has been

108.

repeatedly demonstrated to effect embryo hatching success so I can safely assume the cost is sizeable.

This therefore raises the question of why female M. mogurnda preferred larger males. As already

discussed, mate choice is costly (Pomiankowski 1987; Iwasa et al. 1991; Pomiankowski et al. 1991) and

especially so in this case, so for female choice to persist there must be benefits to compensate for the

costs associated with mate choice, otherwise it would be more beneficial to mate randomly (Friberg and

Arnqvist 2003). Assuming the measure of preference response is accurate for now, why do female M.

mogurnda prefer larger, more dominant males?

Alternate material benefits

It is generally assumed that stronger, more dominant males are better quality mates (Berglund et

al. 1996) and increased parental care quality is only one possible benefit of mating with them. Parental

care seemed the most likely gain, as females play no role in parental care and males do not provide other

obvious material benefits such as nuptial gifts. Another possible direct benefit of mating with these males,

however, is that they are more likely to protect the female during and after mating. In most taxa, larger

males are more likely to win fights, (e.g., Kotiaho et al. 1997; Hagelin 2002; Lopez et al. 2002; Reichard et

al. 2005) and M. mogurnda are no exception. They are an extremely aggressive species and larger

individuals are better fighters (pers. obs.). Males might therefore protect females during or after spawning

from other aggressive individuals. Another benefit may be that males provide access to superior

resources. Males are very territorial when guarding their eggs, and if males hold territories around

spawning sites, females may benefit from having access to better foraging grounds or better spawning

sites.

Genetic benefits

Indirect genetic benefits could maintain maladaptive female choice if the costs to overall

reproduction success is small. Genetic benefits can lead to choosy females producing more viable and/or

attractive offspring (reviewed in Kokko et al. 2003) and there is a potential genetic benefit if traits that

increase success during male-male competition are heritable (Cordero and Eberhard 2003). The

‘differential resource allocation’ hypothesis predicts a reduction in care from attractive males because

females will increase their parental investment to obtain or retain an attractive mate (Burley 1986) which

presumably results in indirect benefits of mating with that male. Alternately, benefits could be gained by

mating with males that are more genetically complimentary or compatible (e.g., Zeh and Zeh 1996; Brown

1997; 1997; Tregenza and Wedell 2000) due to such effects as increasing major histocompatability

109.

complex heterozygosity (e.g., Hoffman et al. 2007), inbreeding avoidance (e.g., Tregenza & Wedell 2002)

and greater offspring genetic diversity (Garant et al. 2005).

Indirect selection, however, is generally accepted as a weak evolutionary force in comparison to

direct selection on mating preferences (Kirkpatrick 1996; Kirkpatrick and Barton 1997; Houle and

Kondrashov 2002). It is possible that the costs of selecting males that are worse parents are smallas there

was no detectable effect of male attractiveness on any other parental care behaviour, but it is unlikely that

genetic benefits could compensate for this cost.

An alternate interpretation

Several studies on fish have reported a decrease in fanning rate but note that it does not

necessarily result in reduced reproductive success (Sargent and Gebier 1980; Coleman and Fischer

1991; Östlund and Ahnesjö 1998; Jones and Reynolds 1999). Males who fanned for shorter bouts actually

enjoyed increased hatching success in three spined sticklebacks Gasterosteus aculeatus (Sargent and

Gebier 1980), fifteen spined sticklebacks Spinachia spinachia (Östlund and Ahnesjö 1998), bluegill

sunfish Lepomis macrochirus (Coleman and Fischer 1991) and common gobies Pomatoschistus microps

(Jones and Reynolds 1999). Males who fanned for shorter bouts, but more often, enjoyed increased

hatching success implying that the frequency that males fan (not necessarily just the total time fanning)

has a large effect on egg hatching. In this study however, the decrease in fan beat was not matched with

an increased frequency of fanning bout so this explanation is unlikely.

3.4.2. Variation in mate choice

I wanted to see if the males who were preferred in Chapter 2 from traditional mate choice trials

were also preferred using an alternative preference test that is gaining ground as being superior to

traditional tests. Contrary to the results from Chapter 2, females spawned sooner with non-preferred

males. Using a latency to mating measure of female choice (the number of days it took pairs to spawn),

not only did male size have no effect on latency to mating or the number of spawnings, females actually

had shorter latency to mating with non-preferred males than preferred males. There was no effect of

attractiveness on the number of spawnings and no effect of male size on any measure of spawning.

Looking more closely at the data shows that the five males who did not spawn at all were all

preferred males. Interestingly, three of the five males who did not spawn were from pairs where the

smaller male was preferred over the larger male, and there were only four pairs of males where the

110.

smaller male was preferred. In the mate choice trials (see Chapter 2) some females were assigned to

pairs that had males who were significantly larger and smaller than them, so perhaps the mean size of

trialled females was smaller than average in the pairs where the smaller male was preferred. This could

have resulted in artificially smallmales being chosen in those three trials, consequently leading to females

choosing not to spawn with those smallmales in the parental care experiments.

There is a chance that these finding are actually resulting from male exerting mate choice and

delaying or preventing mating with unattractive females. If females are the more competitive sex in this

species, the direction of sexual selection may be the reverse of conventional sex roles i.e. ‘reversed sex

role’; (Gwynne 1991; Vincent et al. 1992; Kvarnemo and Ahnejsö 1996). Sex roles are largely influenced

by the operational sex ratio (OSR) (Emlen and Oring 1977; Clutton-Brock and Parker 1992; Kvarnemo

and Ahnejsö 1996), and the OSR will be skewed towards the sex in which there are more reproductive

adults than the opposite sex (Clutton-Brock and Parker 1992; Kvarnemo and Ahnejsö 1996; Parker and

Simmons 1996; Okuda 1999; Ahnejsö et al. 2001). For example, if suitable spawning sites are scarce for

M. mogurnda, the number of reproductive males will be reduced through the shortage of sites, females will

compete for access to mates, and the OSR may skew towards females (in other words, the sex roles are

reversed). Moreover, the costs of reproduction are much higher for males as they are the sole providers of

care making male mate choice even more probable. Kokko & Monaghan (2001) suggest that the

difference in the cost of breeding between sexes is more important than the OSR in determining the sex

roles and a model by Johnstone et al. (1996) that sex differences in costs of choice are more likely have a

much stronger effect on choosiness.

Alternately, female preference may not actually be for worse fathers because the “preferred”

males in this study may not actually be more attractive that non-preferred males. It is possible that the

female preference responses from traditional choice tests did not tell the whole story. The incongruence of

female preference between the two methods for measuring female choice implies that it is based on more

complex parameters than visual (and possibly chemical) cues, and that its expression into actual

increased mating success for some males over others may not be accurately measured by an indirect

measure such as time association.

Incongruence between the two mating preference tests

More studies are starting to show that simultaneous choice tests are not the most accurate

method of quantifying female choice (Wagner 1998; Shackleton et al. 2005; Cotton et al. 2006a). They do

1 1 1 .

not always exclude male-male interactions that may influence mating success for some males, and those

that do often restrict interactions and cues which can effect the expression of choice (Candolin 1999a;

Nilsson and Nilsson 2000) as female preference may be based on more than one male trait (reviewed in

Candolin 2003). Simultaneously presenting females with two extremes in male phenotype does not

indicate how females respond to intermediates (Wagner 1998). Also, the indirect measures of female

mate choice are usually only assumed to equate to actual mating success (Clark and Biesiadecki 2002).

Latency to mating tests resolves many of these problems (Pilastro et al. 2002), females are allowed full

access to physical and chemical cues males offer, and female mating preference can be determined from

an actual mating.

Are non-preferred males actually more attractive?

So if my time association measure of female choice is inaccurate and the latency to mating test is

more accurate, how does this change the interpretation of the results? Females did not spawn sooner with

larger males so male size does not appear to be a cue of choice. Females may, however, still base their

mating preferences on parental care or a trait correlated with parental care: females spawned sooner with

better fathers (i.e. males that showed higher quality of parental care). Having discounted body size as a

cue, what other cues could females be basing their choice on?

Fanning is the most obvious cue as females spawned sooner with non-preferred males who also

had a higher fan beat rate. Fanning itself has been shown to be a trait for mate choice; sand gobies fan

longer and more frequently in the presence of females (Pampoulie et al. 2004) suggesting the this trait

could also be under sexual selection. Males from many species fan before eggs are in a nest, e.g.,

displacement or ‘courtship fanning’ in sticklebacks (Sevenster 1961). Male Florida flagfish Jordanella

floridae also show fanning behaviour prior to the presence of eggs, and male mating success has been

correlated with both prespawning and early postspawning fanning (St Mary et al. 2001). Fanning care

behaviours can also be an honest signal of male quality. Östlund and Ahnesjö (1998) found that female

fifteen-spined sticklebacks preferred males that court more (which is positively correlated to fan beat rate)

and that males who increased their fin beat rate to a high level lost more weight than males who did not.

Courtship and fan beat rate are therefore condition-dependent traits and appear to provide honest cues

for female choice (Zahavi 1975). Courtship can also signal parental care quality (e.g., Knapp and Kovach

1991; Karino 1995; Östlund and Ahnesjö 1998; Wong 2004).

1 12.

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CHAPTER 4 Foraging behaviour and substrate

discrimination in the northern trout

gudgeon (Mogurnda mogurnda)

4.1 Introduction

Optimal foraging models have proven useful in predicting prey and habitat use by foragers

(Mittelbach 1981; Werner and Mittelbach 1981; Werner et al. 1983; Benkman 1987; Osenberg and

Mittelbach 1989). Optimal foraging theory is devoted to four main types of questions (and the

associated behaviour that animals exhibit): which food types an animal should eat; which patch types

an animal should feed in; how much time an animal should devote to feeding in different patches; and

what pattern or speed of movements an animal should engage in while foraging (reviewed in Pyke et

al. 1977).

The choice of foraging habitat encompasses both the question of which patches an animal

should feed in and of how long they should spend there. Habitats vary in food density and microhabitat

complexity, which will affect the optimal search times (and ultimately the food values per unit of time).

As well as theses specific factors, it is important to remember that many other internal and external

factors can affect habitat choice such as predation risk, social interactions, hunger levels, habitat

structure, reproductive state, dietary constraints and even phylogenetic factors (reviewed in Perry and

Pianka 1997).

4.1.1 Food density and distribution

Optimal foraging theory predicts the movement and behaviour of foragers in relation to food

densities. The ideal free distribution (IFD) states that if all individuals are equally “free” to occupy any

space in the habitat, then in environments where resources have patchy distributions relatively high

quality areas are expected to contain more individuals than relatively low quality areas. This theory

assumes, however, that there are no competitive asymmetries among individual so that all individuals

gain equal access to resources (Fretwell and Lucas 1970). Although most wild populations do not

conform to the assumptions of the IFD model (Inman 1990) the theory has still been very useful for

predicting patterns of foraging behaviour. For example, Milinski (1979) demonstrated that by adding a

food source at different rates on two sides of an aquarium, he could generate an ideal free distribution

among three spined sticklebacks Gasterosteus aculeatus. More recently, Collins et al. (2005) found

124.

that the mean size of marine scavenging fish increased significantly with ocean depth while in non­

scavengers there was a significant decline in size, explaining this dissimilarity in distribution with

simple energetic models that matched the distribution of fish to different patterns of food distribution

for each group.

The assumption that there is no variation in competitive abilities is clearly an over

simplification. Since animals do differ in their competitive abilities, territory distributions are expected to

become ideal despotic, with dominant individuals securing the highest quality territories while less able

competitors are forced into unfavourable habitats. Schneider (1984) also showed that dominance

affected foraging strategies; less dominant individuals suffered more aggression while feeding than

more dominant individuals in while-throated sparrows Zonotrichia albicollis. White-throated sparrows

also show a marked preference for habitat in dense shrubbery, arguably because it provides greater

protection from predators (Grubb and Greenwald 1982). In an experimental study, Schneider (1984)

showed that dominant individuals fed from sites nearer to shelter than less dominant individuals as

their rank allowed them greater access to preferred sites. Interestingly, Schneider (1984) also showed

that predation risk was a greater contribution factor to foraging behaviour than optimal energy intake:

individuals depleted the resources close to the shelter before moving to feeding at sites further from

cover even when such sites provided higher energy intake. This is one example of how maximising

the amount of energy intake per unit time may not be an optimal solution for all animals (Milinski and

Heller 1978; Caraco et al. 1980; Krebs 1980; Sih 1980; van den Berghe el al. 1989).

Milinski (1982) showed the effect of different competitive ability on foraging in three spined

sticklebacks. First, individuals were rated in terms of their relative competitive ability in pairwise

foraging tests. Fish were then presented with large and small Daphnia in such a way that handling and

searching times for different sized prey was the same. Larger prey represented greater energetic gain

per unit time and were more profitable, but they required better foraging skills to catch. The relative

capture proportion was noted for each individual and used as a determinant of competitive ability. Fish

where then allowed to forage in the absence of a competitor. Surprisingly, individuals that were more

competitive still successfully incorporated a higher proportion of large prey in their diet. Less

competitive animals had a similar attack rate on larger prey but were less successful at capturing them

and therefore had a higher proportion of small prey in their diet. Milinkski’s (1982) study therefore

neatly demonstrates the importance of considering individual variation in competitive ability in foraging

models.

125.

4.1.2 Food density and individual variation

Though both optimal foraging theory and IFD have their flaws, it is still reasonable to predict

that individuals forage selectively to maximise their energetic gains within certain constraints. Having

established that variation in behaviour between animals has important effects on foraging success

when animals interact, the ability to recognise and subsequently discriminate between variation in

environments could provide additional selective advantages to more competitive foragers or a means

of compensation for more passive foragers. For example, weaker competitors could avoid areas that

are more likely to attract strong competitors.

The amount of food available in a foraging patch is one factor that determines the benefit that

can be obtained for a given level of foraging cost. Animals that adjust their behaviour accordingly can

maximise their competitive ability and energetic gains. So how does food density affect a forager’s

behaviour? A study on the aquatic insect backswimmer Notonecta hoffmanni showed that foragers

adapted their responses to the spatial distribution of prey (Sih 1982). Juvenile N. hoffmanni spent

more time foraging in patches of higher food density and this increased time in better patches

translated into a higher feeding rate. It is interesting to note, however, that Sih (1982) also showed that

N. hoffmanni did not show “optimal” choice of foraging patches or time allocation and that higher

feeding rate did not translate into higher fitness. Also noteworthy was the fact that older starved

foragers were more efficient foragers than their younger or better-fed counterparts. Hunger has been

shown to be a driving force of foraging effort (Beukema 1968) and this highlights another important

interaction that should be taken into account; between life history (age and previous feeding) and

foraging behaviour. Studies have shown a wide range of responses to variation in resource

abundance in fish. Some studies show no effect of food density on foraging time or risk taking

behaviour (Cerri and Fraser 1983; Fraser and Huntingford 1986; Holbrook and Schmitt 1988). In

contrast, Gilliam and Fraser (1987) showed a positive correlation between risk taking and resource

abundance, while Abrahams and Dill (1989) reported a whole variety of responses in guppies

depending on their sex and the level of predation risk.

Variation in prey size is a different form of food density, as optimal allocation time to be spent

searching for and handling prey will change with the energy return from different sized food items

(Werner and Hall 1974). As mentioned above, in Milinski’s (1982) study on three spined sticklebacks,

larger prey provided a higher net energetic profit when searching and handling times were equal for all

size prey. Several species of generalist feeding fish have been shown to selectively choose food

based on their size (e.g., Ivlev 1961; Galbrait 1967; Brooks 1968; Hall et al. 1970; Munk 1992;

Forrester et al. 1994; Luo et al. 1996; Graeb et al. 2006; Hyvarinen and Huusko 2006). Food size is

126.

important to fish growth and may studies demonstrate a positive relationship between the two (Leeren

1958; Parker and Larkin 1959; Paloheim and Dickie 1966; Graeb et al. 2004; Harter and Heck 2006;

Persson and De Roos 2006). Another example of prey size choice can be found in smallmouth bass

Micropterus doloieuf (Stein 1977). Bass select the smallest size class of crayfish when these are

presented on sand, but intermediate sized crayfish on a pebble substrate. Stein (1977) explained that

this pattern occurred because smaller prey are better hidden on larger substrates and the associated

increase in search time meant a decrease in their value relative to more exposed intermediate sized

prey. This is one of the earliest studies to note that microhabitat variation can effect the distribution

and profitability of different prey.

4.1.3 Microhabitat complexity

The complexity of a microhabitat or substrate has been shown to influence both the density

and detection rate of prey (Eklov and Diehl 1994; Merilaita 2003) and the focus so far has been on

patch choice based on prior experience of food abundance. Is there evidence of a patch choice

preference based on potential food abundance? Prey attempt to minimise mortality by adjusting their

use of microhabitats and behaviour in the presence of a predator (Charnov 1976; Stein and Magnuson

1976), so there will often be a higher density of prey around structurally complex habitats. Can

predators discriminate between microhabitats and do they adjust their behaviour accordingly?

Individuals able to discriminate between substrates should select to forage in areas where prey

encounter rates are higher (Krebs et al. 1981).

The structural composition of foraging grounds affects foraging behaviour. Co-existing fish

species in reef communities have been shown to differ in their substrate preferences and foraging

behaviours (e.g., Clarke 1977; Robertson et al. 1979; Robertson and Lässig 1980; Anderson et al.

1981; Robertson 1984; Ormond and Edwards 1987; Krajewski et al. 2006) with the suggestion that

differences in habitat use between species are important in sustaining biodiversity in these

communities. Different microhabitat structure and substrate have certainly been shown to effect

foraging behaviour and growth rate of juvenile fish (Chan et al. 1997; Peake 1999; Nguyen and

Crocker 2006; Scharf et al. 2006).

Increased macroinvertebrate density is related to increased physical complexity at the

microhabitat level, such as increased abundance of vegetation cover (Rabe and Gibson 1984; Gregg

and Rose 1985; Lodge 1985; Chick and Mclvor 1994; Kurashov et al. 1996). Increased prey density

can also be found around more topographical complexity substrates (Rempel et al. 2000; Cole et al.

2003; Macia et al. 2003; Ellis and Bell 2004) as more structurally and physically complex habitats

127.

provide greater refuge spaces for prey (Kelly 1996; Scharf et al. 2006). Increased prey density around

complex microhabitat may, however, also be the result of a reduction in the predator’s ability to

capture prey by decreasing manoeuvrability or visibility (Werner et al. 1983; Babbitt and Jordan 1996;

Babbitt and Tanner 1998; Baber and Babbitt 2004). Studies in the laboratory have shown that complex

habitats contribute to lower predation vulnerability by interfering with predator search and pursuit

(Nelson and Bonsdorff 1990; Gotceitas and Brown 1993; Gotceitas et al. 1995; Fraser et al. 1996;

Lindholm et al. 1999; Bartholomew et al. 2000) and these findings are supported by studies in the field

(Tupper and Boutilier 1995; Beukers and Jones 1998; Heck et al. 2003). As such, prey encounter and

capture rate are usually negatively related to the increase in structural complexity of the microhabitat

(Savino and Stein 1982; Russo 1987; Diehl 1988; Tatrai and Herzig 1995; Mayer et al. 2001). The

degree to which habitat complexity mediates predation may depend on prey anti-predator responses,

the predator posing the threat, and the quality and quantity of the habitat structure (Diehl 1992; Eklov

1997).

4.1.4 Discriminating between microhabitats

Studies show that prey can discriminate between microhabitats and foraging substrates.

Cryptic colouration is an important anti-predatory trait for many aquatic preys (Endler 1978). In some

studies, stream insects prefer cryptic habitat patches (Clifford et al. 1989; Feltmate and Williams 1991;

Feltmate et al. 1992). Stream bottoms are composition of different rock types, overturned rocks and

fallen leaves with stream insects often being uniform dark in colour so that they are well camouflage

against dark backgrounds. Insects are able to distinguish between differently coloured substrate

patches and some species have been shown to chose darker substrates e.g., the lotic mayfly larvae

(Tikkanen et al. 2000), and tide pool sculpins (Houtman and Dill 1994). Macroinvertebrates are not the

only animals to show substrate discrimination as a mechanism of predator avoidance. Differential

habitat use to avoid predators is common (Fraser and Cerri 1982; Holomuzki 1986; Mittelbach 1986;

Ryer et al. 2004; Scharf et al. 2006). Even prey such as juvenile lemon sharks have been shown to

exhibit differential substrate preference, again probably for predator avoidance (Morrissey and Gruber

1993).

If prey chose habitat patches to maximise camouflage and avoid predators, given that more

complex foraging sites potentially have greater prey density, fish should preferentially forage at sites

that are more physically intricate to maximise their energy gain. So, do predators discriminate between

foraging grounds with difference microhabitat characteristics? If so, do predators choose to forage in

128.

areas with high prey density but lower capture rate? Or do they choose to forage in areas with fewer

potential prey but a higher probability of successful capture?

Fish represent a model system for studying foraging behaviour, particularly patch choice and

habitat experiments, because they are easily acclimatised to laboratory experiments, and their

habitats are straightforward to replicate. In a recent study, Webster and Hart (2004) showed that three

spined sticklebacks Gasterosteus aculeatus can not only discriminate between substrates of differing

structural complexity, but also show a strong preference for more complex substrates. Both

smallmouth bass Micropterus doloieuf and pumpkinseed sunfish Lepomis gibbosus have also been

shown to select different prey depending on the substrate on which they are presented and the levels

of topographical complexity (Stein 1977; Macchiusi and Baker 1991).

Webster and Hart (2004) presented three spined sticklebacks Gasterosteus aculeatus

simultaneously with food items on simple and complex substrates, repeating the experiment with

different densities of food items and used fish with differing hunger levels. The sticklebacks showed a

marked preference for complex microhabitats when food densities were equal between substrates,

and when density was greater on the complex substrate. Webster and Hart (2004) explained the result

as adaptive because increased substrate complexity is associated with higher macroinvertebrate

densities. The opposite preference could have been expected, however, as the increased handling

and searching times of smaller prey in more complex structures could have decreased the associated

value of that food item. The result could lie anywhere along a continuum from net energy being higher

due to increased food density (preference for complex substrate) to higher energy gain from prey that

is easier to see and catch (preference for simpler substrate). I wanted to conduct a similar study to see

if this result was repeatable, and where along the continuum Mogurnda mogurnda would lie.

129.

4.1.5 Aims of this study

Using Mogurnda mogurnda, I investigated whether fish can discriminate between substrates

of differing structural complexity when foraging. M mogurnda are a generalist predator of

macroinvertebrates, feeding on insects, crustaceans, worms, molluscs, fishes and plant materials.

They live in slow moving waters in rivers, creeks and billabongs, congregating around vegetation or

rocks where natural differences in habitat structure occur, which make them an excellent candidate for

this study.

I tested whether individuals preferred foraging grounds with more complex structures that

potentially provide refuge to more prey items. I investigated whether fish showed a preference for

foraging grounds of different structural complexity by manipulating actual prey densities in the two

substrates. Hunger is a driving force of foraging effort (Beukema 1968) and had significant effects on

foraging behaviour in the three spined stickleback (Webster and Hart 2004) so I also investigated

whether an individual’s hunger level affected foraging ground choice. Finally, since I manipulated the

amount and proportion of food available in each substrate I looked at which substrate fish consumed

the most food from (i.e. did they choose the substrate that led to the higher energy gain).

130.

4.2 Methods

As in previous chapters, fish were kept in aquaria at 26° Celsius in climate controlled rooms

on a 14:10 hr day: night illumination cycle. The holding tanks (6’ x 2’ x 2’) where fish were kept

between experiments were connected to sump filters filled with bioballs containing bacteria that break

down waste products in the water. Four holding tanks were used, two for fish before experiments and

two for after experiments. The sexes were housed separately in these holding tanks.

4.2.1 Binary Substrate Choice

I presented focal fish with the choice of a “simple” or “complex” substrate. The “simple”

substrate consisted of fine sand (< 3mm) in a tray on one side of the tank. This presented the fish with

a site that was homogeneous for structural complexity and coloration. The “complex” substrate

consisted of large gravel (longest axis range 5-10mm) and a scattering of large rocks (40mm > 80mm)

which created a site that was heterogeneous for structural complexity and coloration with many

interstitial spaces. The experimental tank had three marked zones similar to the experimental set up in

Chapters 2 and 3 with two “preference” zones (marked by the simple and complex substrate trays)

and a non-preference zone (the area in between the trays). The two trays (each measuring 25cm x 21

cm x 1.5cm) were placed on opposite ends of the tank (measuring 2’ x 1’ x 1’). The central “non­

preference“ area was filled with gravel identical to the gravel used to cover the bottom of the holding

tanks (approximately 7mm) and was not treated as a foraging ground.

I had eight treatment groups each with twelve trials (total n = 96). I caught fish from the stock

tanks and allocated them randomly into one of eight holding tanks, trying to avoid individuals that were

at the extreme ends of the size scale. The eight fish were randomly assigned into two groups and then

to one of four prey density: (1) 0:0, complex: simple (no food on either substrate); (2) 1:3,

complex : simple (6 food items in the simple tray vs. 18 food items in the complex tray); (3) 3:1,

complex : simple (18 items in the simple tray vs. 6 items in the complex tray); and (4) 1:1,

complex : simple (6 items in the simple tray vs. 6 items in the complex tray). Hunger levels were also

manipulated within treatments. For each treatment, one group was fed to satiation 72 hours before the

trial and the other group was fed to satiation one hour before the trial.

The food used in the experiment was the protein pellets that were the fish’s sole diet so that

they were familiar with the food being offered. I set the trays in the tank, added the food at random

points on the tray then carefully filled the tank with water to begin the experiment. Each trial consisted

of placed one fish under a clear container in the centre of the non-preference zone between the two

131 .

trays for a five minutes acclimatisation period to ensure that it could see both substrates. After five

minutes, I carefully lifted the container covering the fish and started recording their position in the tank

for ten minutes. Using JWatcher™ (Blumstein et al. 2000), I recorded how often each fish entered a

zone, how long each fish was in each zone and how many feeding strikes each fish made in each

zone. After ten minutes, I caught the fish and housed them in a used stock tank. I then used a vacuum

gravel cleaner to remove at least half a tank of water, and if the treatment included food items I

removed any uneaten food particles. I then added food at random points which would sink to the

bottom for the next trial, and carefully refilled the tank.

I swapped the trays between the opposite ends of the tank after half of the trials (n = 6) within

each treatment. I tried to reduce the number of times I shifted the trays because it was difficult to do

without disturbing the substrate topography and I wanted to keep the presentation of the substrates as

similar as possible throughout the experiments.

4.2.2 Statistical Analyses - Foraging Analysis

In the analysis of substrate preference, I considered the following variables:

• The number of visits was the number of times a fish entered a substrate preference zone.

• The total duration was the total amount of time a fish spent in a substrate preference zone.

• The mean duration was the average duration per visit a fish spent in a substrate preference

zone.

• The duration proportion was the proportion of time a fish spent in a substrate preference

zone relative to the total duration of the observation period (10 minutes).

• The relative proportion was the proportion of time a fish spent in a substrate preference zone

relative to the time a female spent in both preference zones (excludes the time in the non­

preference zone).

I used one-sample t-tests to quantify the effect of substrate on the response variables. If there

was no significant difference in the response variables between the substrates, a t-test would show

that the difference between the values for the two substrates (e.g., complex - simple substrate) did not

differ significantly from zero. I tested for a difference between substrates in the number of visits, total

duration of time spent on each substrate and the mean duration of each visit. In my analyses, I used

the difference in values between the substrates because this provides a simple way to analyse and

present the data. This method of analysis takes into account that the use of substrates is mutually

exclusive, and the aim of the experiment is to detect a difference in usage between the two substrates.

132.

I also used general linear models with sex, feeding treatment and hunger level as fixed factors

to test for their effect on the number of visits, total duration of time spent on each substrate and the

mean duration of each visit. For these models, I again used the difference between substrates for

each variable (e.g., difference in number of visits to the complex substrate minus the number of visits

to the simple substrate). I used the difference in values rather than including substrate as a fixed factor

in the models because this makes it easier to detect the main effect of the treatment rather than

having to test for interactions (e.g., a treatment*substrate interaction because the food density on

substrate types differs between treatments so the preferred substrate should vary between

treatments). I also tested for the effect of sex, feeding treatment and hunger level on the relative

proportion of time spent in one substrate preference zone compared to the total time spent in both

preference zones (i.e. total time excludes time spent in the non-preference zone). I used the

proportion of time on the complex substrate. Assumptions of normality were tested for, and satisfied,

in all the models.

I also repeated the models but used only data from treatments 2 (food ratio of 1:3 for

complex : simple) and treatment 3 (food ratio of 3:1 complex : simple). I repeated the model (with

feeding treatment and hunger level as fixed factors) because these two treatments showed the

greatest extremes in the difference in food ratio between the two substrates. It was therefore more

likely than I would detect a treatment effect than in the case where I included the two treatments with

equal food ratio per substrate (as these two treatments should not differ). I tested for sources of

variation in the number of visits, difference in total time spent on a substrate and the mean duration of

each visit as well as the relative proportion of time spent on each substrate. I did not include sex in the

models with the reduced data set because the analysis on the full data set indicated that there was no

effect of sex on substrate-based foraging decisions.

I also conducted separate one-sample t-tests on the relative proportion of time spent on the

complex substrate for each treatment and hunger level. Finally, I used Mann-Whitney U tests to look

for an effect of treatment and hunger level on the total number of feeding strikes on each substrate.

133.

4.3 Results

There was no evidence of a foraging preference for either the complex or the simple substrate

(Table 4.3.1). The t-tests showed there was no significant difference in the use of complex and simple

substrates. There was no difference in the number of visits, total time on each substrate or the mean

duration of each visit. There was also no effect of treatment or hunger level on the number of visits,

total time or the mean duration of visits to each substrate. There was, however, a significant difference

between the sexes for the mean duration of visits to complex versus simple substrates (Table 4.3.2,

Fig 4.3.1: F = 9.849, df = 1, p = 0.002). Females preferred the complex substrate (Fig. 4.3.2; t = -

2.989, df = 47, p = 0.004) while males showed no preference for either substrate (Fig. 4.3.3; t = 1.566,

df = 47, p = .124).

There was no significant difference between the sexes in the difference in the number of visits

or total time spent on each substrate, but looking at the difference in the mean total time spent on

each substrate among the treatments does suggest a treatment effect (Fig. 4.3.4). Small sample sizes

make it difficult to detect a statistically significance result so this could be worthy of future

investigation. There was no difference in the relative proportion of time spent on each substrate

between the sex, among treatments or between hunger levels.

Analysing only treatments 2 and 3, individuals still showed no foraging preference for either

the complex or the simple substrate (Table 4.3.3). There was no effect of treatment or hunger level on

the number of visits, total time or mean duration of visits to each substrate type. There was also no

effect of treatment or hunger level on the relative proportion of time spent on each substrate (Table

4.3.4).

There was, however, a difference in the number of feeding strikes between hunger levels

across treatments (Table 4.3.5). There were no feeding strikes for treatment 1 (as there was no food

present) but there were also no strikes for fish fed to satiation one hour before the trial (Fig. 4.3.5).

The treatment by hunger interaction effect was due to difference between treatment 1 and the other

treatments, as there were large numbers of feeding strikes in fish fed 72 hours before the trial in

treatments 2, 3 and 4 but not in treatment 1.

134.

Table 4.3.1 The difference between the two substrates for the listed response variables measured as

response variable for complex substrate minus response variable for simple complex (n = 96 for all

variables). The response variables are the number of visits, total time spent on each substrate and the

mean duration of each visit. Difference is measured as response variable for complex substrate minus

response variable for simple complex. A significant bias towards the use of a substrate occurs if the

mean difference is greater or less than zero (one-sample t-tests).

Response Variable Mean ± SD t df Sig.

Difference in Number of Visits 0.20 ± 2.25 0.863 95 0.390

Difference in Total Time Duration (sec) -19.19 ±206.25 -0.912 95 0.364

Difference in Mean Duration (sec) -5.11 ±604.00 -0.829 95 0.409

135.

Table 4.3.2 General linear models with sex, feeding treatment and hunger level (HL) as fixed factors

(n = 96 for all variables). Number of visits, total time spent on a substrate and mean duration of each

visit were measured as the difference between complex minus simple substrates. The relative

proportion of time on each substrate was the proportion of time spent in one preference zone

compared to the total time spent in both preference zones (excludes time in non-preference zone).

Variables marked * are significant.

Response Variable Factor df F Sig.

Difference in Number of Visits Sex 1,90 1.961 0.165

Treatment 3, 90 0.138 0.937

HL 1,90 1.487 0.226

Difference in Total Time Duration Sex 1,90 2.150 0.146

T reatment 3, 90 0.506 0.679

HL 1,90 0.000 0.997

Difference in Mean Duration Sex* 1,90 9.849 0.002*

T reatment 3, 90 0.607 0.612

HL 1,90 0.006 0.940

Relative Proportion of Duration Sex 1,90 1.332 0.251

T reatment 3, 90 0.223 0.881

HL 1,90 0.208 0.649

136.

Table 4.3.3 General linear models with feeding treatment and hunger level (HL) as fixed factors only

for treatments 2 (food ratio of 1:3 complex : simple) and 3 (food ratio of 3:1 complex : simple). N = 96

for all variables). Number of visits, total time spent on a substrate and mean duration of each visit were

measured as the difference between complex minus simple substrates. The relative proportion of time

on each substrate was the proportion of time spent in one preference zone compared to the total time

spent in both preference zones (excludes time in non-preference zone).

Response Variable Factor df F Sig.

Difference in Number of Visits Treatment 1 0.060 0.808

HL 1 1.207 0.278

Difference in Total Time Duration T reatment 1 0.452 0.505

HL 1 0.004 0.951

Difference in Mean Duration T reatment 1 0.832 0.367

HL 1 0.151 0.699

Relative Proportion of Duration T reatment 1 0.148 0.702

HL 1 0.063 0.804

137.

Table 4.3.4 General linear models split by feeding treatment and hunger level (HL), n = 96 for all

variables). The relative proportion of time on each substrate was the proportion of time spent in one

preference zone compared to the total time spent in both preference zones (excludes time in non­

preference zone). Feeding treatments were: (1) 0:0, complex : simple (no food on either substrate); (2)

1:3, complex : simple (6 food items in the simple tray vs. 18 food items in the complex tray; (3) 3:1

complex : simple (18 food items in the simple tray vs. 6 food items in the complex tray); (4) 1:1,

complex : simple (6 food items in the simple tray vs. 6 food items in the complex tray). Hunger level 1

was feeding fish to satiation 72 hours before the trial and hunger level 2 is feeding fish to satiation one

hour before the trial.

Response Variable T reatment HL t df Sig.

Relative Proportion of Duration 0:0 1 -0.219 11 0.830

2 -0.187 11 0.855

1:3 1 0.787 11 0.448

2 -0.829 11 0.425

3:1 1 -0.102 11 0.921

2 0.790 11 0.446

V.1 1 -0.187 11 0.855

2 -8.290 11 0.425

138.

Table 4.3.5 The comparison of the total number of feeding strikes during the 10 minute observation

period for hunger levels within each treatment (Mann-Whitney) (n = 96 for all variables). Feeding

treatments were: (1) 0:0, complex : simple (no food on either substrate); (2) 1:3, complex : simple (6

food items in the simple tray vs. 18 food items in the complex tray; (3) 3:1 complex : simple (18 food

items in the simple tray vs. 6 food items in the complex tray); (4) 1:1, complex : simple (6 food items in

the simple tray vs. 6 food items in the complex tray).Treatments marked * are significant. Hunger level

1 was feeding fish to satiation 72 hours before the trial and hunger level 2 is feeding fish to satiation

one hour before the trial.

Response Variable Treatment Mean ± SD U Z Sig.

Total Feeding Strikes 0:0, complex : simple

HL1 - 0.00 ± 0.00

HL2 - 0.00 ± 0.00 72.00 0.000 1.000

1:3, complex : simple:*

HL1 - 0.00 ± 0.00

HL2 - 2.75 ± 2.05 96.00 -3.599 0.000*

3:1, complex : simple*

HL1 -0 .0 0 ±0.00

HL2 - 4.58 ±2.31 78.00 -4.459 0.000*

1:1, complex: simple*

HL1 - 0.00 ± 0.00

HL2 - 2.92 ± 2.39 96.00 -3.591 0.000*

139.

Diff

eren

ce i

250 -

ao

<rsu3Q

4>

a

0 “

o

-250 -o

jFemales

.I...Males

Sex

Figure 4.3.1 The difference in mean duration of visits to the complex versus simple preference zones

for each sex (F = 9.849, df = 1, p = 0.002).

140.

Freq

uenc

y

14 H

12 - j

-250 -200 -150 -100 -50 0 50 100 150 200 250

Difference in Mean Duration (sec)

Figure 4.3.2 Difference in mean duration of visits by females to the complex versus simple substrate

zones (one-sample t-test; t = -2.989, df = 47, p = 0.004). Overall, females spent less time on the

complex substrate.

141.

Freq

uenc

y

Difference in Mean Duration (sec)

Figure 4.3.3 Difference in mean durations of visits by males to the complex versus simple substrate

zones (one-sample t-test; t = 1.566, df = 47, p = 0.124). There was a non-significant trend for males to

spend more time on the complex substrates.

142.

-20 -

-40 -

-60 -

Feeding Treatment

Figure 4.3.4 The means for the difference in total time spent on the complex versus simple. Feeding

treatments are: 0:0, complex = simple (no food on either substrate); 1:1, complex = simple (6 food

items in the simple tray vs. 6 food items in the complex tray); (3) 1:3, complex = simple (18 food items

in the simple tray vs. 6 food items in the complex tray); (4) 3:1, complex = simple (6 food items in the

simple tray vs. 18 food items in the complex tray).

143.

5 * r __<b J t

♦ P N

o 4 Hasc3 1 _£

oH 1 —

1 -

0 - e © © ©

0:0 1:3 3:1Feeding Treatment

1:1

Figure 4.3.5 The mean ± SE for total number of feeding strikes per individual in the four feeding

treatment clustered by hunger level. Circles designate huger level 1 where fish were fed one hour

before the trial, and triangles designate hunger level 2 where fish that were only fed three days before

the trial. Feeding treatments were: (1) 0:0, complex : simple (no food on either substrate); (2) 1:3,

complex : simple (6 food items in the simple tray vs. 18 food items in the complex tray; (3) 3:1,

complex : simple (18 food items in the simple tray vs. 6 food items in the complex tray); (4) 1:1,

complex : simple (6 food items in the simple tray vs. 6 food items in the complex tray).

144.

4.4 Discussion

In the previous chapters, I discussed the costs of reproduction: the costs of mating (Daly

1978; Pomiankowski 1988; Iwasa et al. 1991), of mate choice (Hedrick and Dill 1993; Rowe 1994;

Grafe 1997; Watson et al. 1998) and of parental care (e.g., Stanley 2002). In light of this, the

processes whereby animals obtain energy for these activities becomes of interest, especially when

discussing traits that are condition-dependent (Zahavi 1975; Getty 1998). Both optimal foraging

models (reviewed in Pyke et al. 1977; and Schoener 1986) and ideal free distribution theory (Fretwell

and Lucas 1970) discuss individual foraging behaviour in terms of food density. Though these theories

are somewhat oversimplified, it is still reasonable to follow their predictions that individuals will forage

selectively to maximise their energetic gains.

Different habitat structures present animals with differences in food density and detection rate

of prey (Eklov and Diehl 1994; Merilaita 2003). There will often be a higher abundance of prey around

structurally complex habitats (Charnov 1976; Stein and Magnuson 1976) so predators might be

expected to prefer foraging in patches of greater structural complexity. For example, both smallmouth

bass Micropterus doloieuf and pumpkinseed sunfish Lepomis gibbosus select different prey depending

on the substrate on which they are presented and the differing levels of topographical complexity

(Stein 1977; Macchiusi and Baker 1991). Different microhabitat structure and substrate have been

shown to affect the foraging behaviour and growth rate of juvenile fish (Chan et al. 1997; Peake 1999;

Nguyen and Crocker 2006; Scharf et al. 2006).

There was no overall effect of habitat complexity (substrate) on foraging preference in

Mogurnda mogurnda. Females, however, showed a preference for simple substrates while males

showed none. There was no interaction effect of sex on treatment or hunger level, indicating this was

a general trend across the various experimental groups. It is unclear why females should display this

preference but males should not. (Abrahams and Dill 1989) reported a variety of responses in guppies

depending on their sex and the predation risk level, and other studies have shown a wide range of

responses to variation in resource abundance from no effect of food density (Cerri and Fraser 1983;

Fraser and Huntingford 1986; Holbrook and Schmitt 1988) to a positive correlation (Gilliam and Fraser

1987). It possible that females could have been at a stage in their reproductive cycle where they were

producing eggs and the higher energetic expenditure led them to a foraging strategy that maximised

the number of food items. Food items were easier to find in the simple habitat, thus lowering searching

and handling time and increased the number of successful food strikes. As the preference was not

detectable across all individuals, I consider this a weak preference trend but this results highlight the

145.

fact that individual variation should be taken into account in such studies; foraging behaviour can be

influenced by many factors such as predation risk, social interactions, reproductive state, and even

phylogenetic factors (reviewed in Perry and Pianka 1997).

There was a clear interaction between the effect of hunger level and food density on the

number of food strikes between substrates. There were no feeding strikes for treatment 1 (as there

was no food present) but there were also no strikes for fish fed to satiation one hour before the trial.

The difference lay between treatment 1 and the other treatments, as there were large numbers of

feeding strikes in fish that had not been fed for three days before the trial in treatments where food

was present. Hunger has been shown to be a driving force of foraging effort (Beukema 1968; Sih

1982). My result supports the fact that M. mogurnda showed no substrate preference rather than they

were simply non-responsive to the experiment and disinterested in feeding.

In a recent study, Webster and Hart (2004) showed that hunger-motivated three spined

sticklebacks Gasterosteus aculeatus prefer to forage in complex substrates. My results are not

equivalent to their findings, as hungry sticklebacks showed a marked preference for complex

microhabitats when food densities were equal between substrates, and when density was greater on

the complex substrate. Consistent with my results, however, satiated fish showed no preference, nor

was there a preference for complex substrates when food density was higher on simple substrates.

Webster and Hart (2004) explained their results as adaptive because increased substrate complexity

provides more refuges for prey, and is associated with higher macroinvertebrate densities (Kelly 1996;

Scharf et al. 2006). Increased prey density around complex microhabitat has, however, also been

explained by a reduction in predator’s ability to capture prey by decreasing manoeuvrability or the

visibility (Babbitt and Jordan 1996; Babbitt and Tanner 1997; Baber and Babbitt 2004). This has been

supported by studies in the laboratory (Nelson and Bonsdorff 1990; Gotceitas and Brown 1993;

Gotceitas et al. 1995; Fraser et al. 1996; Lindholm et al. 1999; Bartholomew et al. 2000) and in the

field (Tupper and Boutilier 1995; 1997; Beukers and Jones 1997; Heck et al. 2003). As such, prey

encounter and capture rates are usually negatively correlated to the increase in structural complexity

of the microhabitat (Savino and Stein 1982; Russo; 1987; Diehl 1988; Tatrai and Herzig; 1995 Mayer

et al. 2001).

A reverse preference or no effect of substrate could therefore also be predicted as the

increased handling and searching times of smaller prey in more complex structures could decrease

the associated value of a food item. Optimal foraging theory predicts that allocation time spent

searching for and handling prey will change the energy return for different sized food items (Werner

and Hall 1974) with larger prey presenting a higher net energetic profit when searching and handling

146.

times are equal for all sizes (Milinski 1982). Searching and handling times are rarely equal, however,

and are certainly not in structurally different microhabitats. In addition, prey employing cryptic

colouration have been shown to prefer darker substrates e.g., the lotic mayfly larvae (Tikkanen et al.

2000), and tide pool sculpins (Houtman and Dill 1994). If the diet of M. mogurnda includes cryptic

species of prey that choose habitat patches to maximise camouflage and avoid predators, the further

increase in searching and handling time may reduce a preference for complex substrates.

Habitat aside, several species of generalist feeding fish have been shown to selectively

choose food based on their size (e.g., Ivlev 1961; Galbrait 1967; Brooks 1968; Hall et al 1970; Werner

and Hall 1974; Munk 1992; Forrester et al. 1994; Luo et al. 1996; Hyvarinen and Huusko 2006).

Recent foraging models are more comprehensive, and awareness of the complexities of the demands

of an organism has increased. Empirical studies are developing to further explore foraging theory.

Ultimately, the degree to which habitat complexity mediates predation may depend on prey

antipredator responses, the predator posing the threat, and the quality and quantity of the habitat

structure (Diehl 1992, Eklöv 1997).

147.

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CHAPTER 5 General Discussion

5.1 Aims of this study

In this study, I aimed to measure and quantity what traits female Mogurnda mogurnda

preferred in relation to male size and fighting ability. There is growing acceptance that the previously

assumed positive correlation between attractiveness and male size/dominance is not always correct.

The results of my simultaneous choice test imply, however, that females do in fact prefer larger males.

I feel confident inferring that preferred males are more dominant, as this species is very aggressive

and observational data clearly shows that larger individuals win more fights. Interestingly, I found

evidence of size assortative mating with larger females tending to spend more time with larger than

smaller males, and I also found that that larger females exhibited a stronger preference for the

preferred male than smaller females, implying that female choice in this species is condition-

dependent.

In the recent literature, however, the accuracy of simultaneous choice tests has been called

into question. I aimed to compare the expression of female mate preferences from a traditional

association preference tests to a method of assessing choice that has been gaining ground in recent

years: latency to mating tests. Often when the results of association preference tests are compared to

latency tests, either preferred characteristics are no longer preferred or different characteristics

become indicators of male attractiveness. I found the male trait that was preferred in traditional tests

(male size) were not preferred in latency tests, supporting this view. At this point, I wish to clarify the

terminology I will use in this discussion due to female choice being judged on two different

methodologies and that led to opposing results. I will continue using “preferred” and “non-preferred”

when discussing the males chosen under traditional choice tests in Chapter 2, but I will refer to males

chosen by the latency to mating test as “mated” and “non-mated” males. I chose this terminology

because the trend of females taking longer to spawn with preferred males was largely due to five

preferred males failing to spawn in the allotted time.

Another aim was to identify any traits that honestly signalled male parental quality and

whether females were choosing males based on these characteristics. I found no correlations between

male size and parental care. Fan beat rate was the only parental care behaviour that correlated with a

male trait, and is was negatively correlated with female preference itself, and so was a dishonest

signal of care. In the latency to mating tests, it is unclear what traits females based their preference

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response on, but since they spawned sooner with non-preferred males who showed higher quality

parental care than preferred males, females could still be choosing males based on a trait correlated

with quality of care. (Note: in this chapter, I will conceptually treat male attractiveness as a trait

because if it is correlated to one or more variable phenotypic traits that females base their choice on

which is a sound assumption otherwise females would not be discriminating between males). Male

attractiveness could be treated as a trait when looking for effects on care behaviour.

Finally, with the focus on so many energetically expensive activities I decided to examine one

aspect of foraging in M. mogurnda: patch choice and substrate discrimination. I found that there was

no preference for the greater potential for food presented by the higher incidence of interstitial spaces

in “complex” substrates. The only preference I found was by females but it was for “simple” substrates,

which was the opposite result from a recent paper that conducted a similar study. Potential prey

density is not the only factor influencing foraging behaviour, however, and the increased search and

handling time associated with prey in complex microhabitats and the lower energetic award from

smaller prey items may have balanced the value of seeking prey on complex and simple substrates.

5.2 Condition-dependent female choice

The discovery that female choice in this species is potentially condition-dependent is exciting.

This species satisfies two predictions of condition-dependence (stronger preference in larger females

and size assortative mating) while empirical evidence to support this theory is still scarce. Size-

assortative mating itself is common across taxa in fish, such as cichlids (Barlow et al. 1990; Budaev et

al. 1999), and coral gobies Paragobioon echinocephalus (Kuwamura et al. 1993). Condition-

dependent female choice theory predicts that better quality females exhibit stronger preferences for

the same costs as lower quality females and therefore have better mates through either more intense

searching or having a higher rejection rate than lower quality females.

Finding of stronger expression of preference in larger females is not uncommon, however.

Notable examples include guppies Poecilia reticulata (Lopez 1999; Syriatowicz and Brooks 2004),

three spined sticklebacks Gasterosteus aculeatus (Bakker et al. 1999), upland bullies Gobiomorphus

breviceps (Poulin 1994) and deep-snouted pipefish Syngnathus typhie (Mazzi 2004). Mate preference

is predicted to be differentially costly with respect to female quality (Cotton et al. 2006) with higher

quality females suffering lower costs for a given mate preference, or are able to be more discerning for

the same cost, than poorer quality females. By much the same mechanism that secondary sexual

ornaments are predicted to be condition-dependent, female mating preferences are predicted to be

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weaker when the costs are higher so the strength of female preference is expected to vary with female

condition (Pomiankowski 1987; Grafen 1990; Iwasa et al. 1991; Iwasa and Pomiankowski 1999).

Interestingly, honest signaling of male secondary sexual characteristics may be partially affected by

female condition-dependence (Cotton et al. 2006). Mate preferences for honest signals should be

more beneficial for high quality females if low quality females have less to gain from discrimination. For

example, in a species where male display rate honestly signals male investment in parental care, high

quality females who can produce more offspring than the average male can care for should prefer

well-ornamented mates, as this will directly increase their fitness. Lower quality females whose

maximal egg production is smallenough that an average male could care for them would have less to

benefit from expressing this mating preference and would more likely to mate randomly to avoid

paying the costs of mate choice (Cotton et al. 2006).

5.3 Parental care behaviours in M. Mogurnda

Individuals are expected to maximise their overall reproductive success by trading off

investment between current and future reproductive events (Winkler 1987). Parents are expected to

adjust parental care in relation to their own fitness, because parental care is demonstrably costly (e.g.,

Drent and Daan 1980a; Stanley 2002; Hanssen et al. 2003). Body condition is an important factor

affecting the quality of parental care an individual can provide, so it is reasonable to expect larger

individuals in better condition to be better quality parents. I did not, however, find this to be the case in

my study of M. mogurnda.

I found no relationship between male size and any of the measured parental care behaviours:

fanning, guarding, filial cannibalism or the resulting hatching time. Fanning is a particularly expensive

care behaviour, especially under sup-optimal condition such as low dissolved oxygen levels (Hale et

al. 2003; Lissaker et al. 2003). There may not have been any difference in fanning behaviours

between males of different sizes because of the favourable conditions in the breeding tanks. Oxygen

levels and water quality remained high at all times, requiring relatively low effort from males to care for

the eggs. The very low proportion of whole filial cannibalism (13.1%) supports this, and these

incidences were almost certainly due to human disturbance as they almost always occurred the day

after I recorded parental care behaviours. Partial filial cannibalism has been suggested to helps

parents recover the energetic costs of parental care (Rohwer 1978) and there were no recorded partial

filial cannibalisms, suggesting that care under these conditions were not particularly expensive. There

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also may not have been enough difference in condition between large and smallmales to detect

differences in care, as I fed fish a reasonable amount of food every two days.

I also found no difference in any of the parental care behaviours between preferred and non­

preferred, except for fanning rate. It was unexpected to find that preferred males fanned at a lower

rate. As already discussed, this poses a dilemma as it makes female choice maladaptive, with females

actually suffering a cost of decreased male care from their mating preference. This leads to the

question of how female choice is maintained in this species if females are incurring higher costs for

their mating preferences. There are several possible explanations for the discovery of maladaptive

female choice in this study; females could be gaining material benefits unrelated to parental care;

females could be gaining genetic benefits, or there is the alternate interpretation that my method for

discriminating female preference is inaccurate.

5.4 Maintaining a maladaptive preference

I found no difference in any of the parental care behaviours between preferred and non­

preferred, except for fanning rate. I did not expect to find that preferred males were lower quality

parents, as the most obvious benefit from female choice in this species would seem to be improved

parental care because females receive little else from males. An increase in female reproductive

output offers the most straightforward explanation as to how mate choice benefits outweighs the costs

of choice (Iwasa and Pomiankowski 1999), which explains why it has been the main focus of research

in many studies (e.g., Pizzari 2003; Wagner and Harper 2003). Female choice is a powerful tool of

sexual selection, having been suggesting as the driver for the evolution of exclusive paternal care in

arthropods (Tallamy 2000) and territorial fish (Ah-King et al. 2005). I discussed other potential material

and genetic benefits in Chapter 3, and females could receive a mixture of direct and indirect benefits

to help compensate for the costs of mate choice (Cordero and Eberhard 2003; Kokko et al. 2003).

There is also the possibility that the sensory bias model of choice may be maintaining female choice

(West-Eberhard 1984; Ryan and Rand 1990; Endler and Basolo 1998; reviewed in Fuller et al. 2005).

It has the benefit of being applicable to instances of maladaptive choice (Rice and Holland 1997;

Holland and Rice 1998) such as this one, and females may still accrue benefits from better-quality

mates. Unfortunately, however, there is no direct evidence from my study to support this model of

female choice.

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5.5 Comparing female choice tests

The most obvious answer to the appearance of maladaptive choice in this study is that

female’s may not actually prefer worse fathers because the preferred males in this study may not

actually be more attractive that non-preferred males. There is growing evidence that simultaneous

choice tests are not the most accurate method of discriminating female choice (Wagner 1998;

Shackleton et al. 2005; Cotton et al. 2006). It is possible that the use of female preference responses

from traditional choice tests simply did not tell the whole story. The incongruence of female choice

between the two methods of measuring female choice implies that mating preferences are based on

parameters that are more complex than visual (and possibly chemical) cues (Candolin 1999a; Nilsson

and Nilsson 2000). Choosing who to associate with who to actually mate with could be quite different

decisions, and the expression of choice based on association into actual increased mating success

might reflect this.

5.6 Variation in expression of mating preference

It is quite plausible that females show a context dependent expression of choice. When

restricted from mating cues and interactions, females may chose to associate with the larger male in a

non-reproductive context, or male size may only be one of many preference cues. As already

discussed, M. mogurnda are an aggressive species and males might protect females from other

aggressive individuals during or after spawning. Females might also initially choose larger males if

they provide access to superior resources, such as better foraging grounds or better spawning sites.

In a mating context where females have access to the whole gamut of cues and interactions, they may

select using different criteria. A size-based preference might diminish if females can read cues that

imply larger males provide lower quality parental care (Forsgren 1997; Wong 2004), are likely to

transmit diseases (Freeland 1981) or are sperm depleted (Pitnick and Markow 1994; Preston et al.

2001).

Females were quite young (though all were old enough to be identified as females which

means they are of reproductive age) when the first association trials were conduction. This may have

had an effect. Clement et al. (2005) showed that differences in female reproductive state correspond

to changes in female affiliation with males. In the African cichlid fish Astatotilapia burtoni, gravid and

non-gravid females were given the choice of associating with territorial (reproductively active) or non­

territorial males. Gravid females preferentially associated with territorial males, whereas non-gravid

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females showed no preference. This study highlights that reproductive state of both males and

females could be an important factor in the expression of mating preferences.

As discussed in Chapter 3, the incongruence between the two results could be due to sex role

reversal. The delay in spawning time (including the five pairs who did not spawn at all) could be

explained as being a consequence of males exerting mate choice and delaying or preventing mating

with unattractive females. Male M. mogurnda invest heavily into offspring by guarding them (possible

to the detriment of foraging which will reduce their condition) while females only provide eggs. If a

restricting factor such as suitable spawning sites is scarce, the operational sex ratio (OSR) may skew

towards females and sex roles are largely determined by OSR (Emlen and Oring 1977; Clutton-Brock

and Parker 1992; Kvarnemo and Ahnejsö 1996). The difference in the cost of breeding between

sexes, however, appears theoretically to be more important than the OSR in determining the sex roles

in many cases (Johnstone et al. 1996; Kokko and Monaghan 2001). The sex differences in this

species in terms of costs of choice are therefore are very likely to have a strong effect on choosiness.

5.7 Cues to mating preference

The only detectable relationship between parental care and male attractiveness (as defined by

association trials) was a negative one. The latency to mating measure of female choice, however, may

be a more accurate measure of choice, which changes the interpretation of my results. Using the

spawning time measure of choice, females showed no preference for male size. Mated males (defined

as the males females spawned with) were also the non-preferred males from the mate choice

experiment and the non-preferred males fanned at a higher rate. So, even though there was no

obvious cues as to why females preferred mated males, this indicates that mated males are better

quality parents. Female may then still be basing their mating preferences on parental care or a trait

correlated with it.

Possible other cues for female choice could be fanning itself, as it has been shown to be a

trait for mate choice (e.g., Sevenster 1961; St Mary et al. 2001; Pampoulie et al. 2004) and could also

be an honest signal of male quality (Östlund and Ahnesjö 1998). It is logical that females base their

preference on a trait that honestly signals condition, as condition will effect the quality of parental care.

There is a great deal of literature on the correlation between sexual displays and parental investment

showing positive (e.g., Linville et al. 1998; Candolin 2000; Senar et al. 2002; Voltura et al. 2002; Kolm

2004; Halupka and Borowiec 2006), negative (e.g., Qvarnström 1997; Wong 2004; Mitchell et al.

2007) and no relationship (e.g., Mountjoy and Lemon 1997; Smiseth et al. 2001). This species

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displays no obvious secondary sexual traits, but signals of parental care need not necessarily be

sexually selected traits. For example, male three spined sticklebacks have larger pectoral fins than

females, which females can use as a cue to male parental quality (Bakker and Mundwiler 1999).

Finally, with the focus of so much of this study on energetically expensive activities like mate

searching, mate choice, mating, and parental care I turn to the means of maintaining condition and

obtaining energy for these activities.

5.8 Foraging

The efficiency with which individuals gain energy is of immense importance and affects their

competitiveness in competition (e.g., dominance struggles) and the expression of traits that are

condition-dependent (e.g., honest signals of quality). As discussed earlier, different habitat structures

present animals with differences in food density and associated food values, such as search times and

there will often be a higher abundance of prey around structurally complex habitats (Charnov 1976);

Stein & Magnuson 1976). Predators might therefore be expected to prefer foraging in patches of

greater structural complexity, such as in Webster and Plarts’ (2004) study on three spined sticklebacks

Gasterosteus aculeatus. The sticklebacks spent more time foraging in complex microhabitats when

food densities were equal between substrates, and when density was greater on the complex

substrate. In my study, I did not find a clear preference for either zone in M. mogurnda. Females did

show a preference for simple substrates (based on one of several measure of association) while

males showed no preference at all. Although increased structural complexity hides a potentially higher

prey density, the prey will have an associated increase in handling and searching times and this will

decrease the net energetic value of prey and therefore the net intake of energy for that patch. It could

also be that the fish used in this experiment were quite young when they were caught and may not

have leaned which habitat patches have greater abundances of prey. Ultimately, the degree to which

habitat complexity influences foraging behaviour depends on a complex suite of factors, such as prey

antipredator responses, the foraging ability of the predator, and the quality and quantity of the habitat

structure (Eklöv and Diehl 1994).

180.

5.9 Conclusion

Fish are an under utilised model system for studies of mate choice and parental care. They

present unique opportunities because they are the most numerous and varied of the vertebrates and

show a wide range of often dynamic care patterns ranging from no-care, to uniparental, paternal and

maternal care (Gross and Sargent 1985; Reynolds et al. 2002). If fish biologists are to work on a

species that is not well-known like guppies or sticklebacks, they need to spend a lot of time learning

about the fish they are studying. This study has made some interesting discoveries and posing some

even more interesting questions that I am unable to answer because I do not have sufficient data on

the natural breeding system, detailed information about the mating and care behaviours, and most

importantly the relative costs and benefits of these behaviours. I think Mogurnda mogurnda shows the

potential for being an exciting species to examine in terms of empirical studies on mate choice and

parental care. The first step would be to study this species in the wild to learn how to apply the

theoretical background I have outlined in this thesis. Physiological measures of the costs of care,

particularly along environmental gradients such as those associated with oxygen and turbidity, would

address aspects of the literature that have not yet been comprehensively covered. I think this species

is highly suited to such studies.

181 .

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