Effects of water temperature on life-history traits of selected South African aquatic insects

342 Pages·2014·10.39 MB·English

Effects of water temperature on life-history
traits of selected South African aquatic
insects

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By w
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Vere Ross-Gillespie

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Supervisors: Dr. Helen Fi. Dallas, Emeritus Associate Professor
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Jenny A. Day andr Associate Professor Mike. D. Picker
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Thesis presented for the Degree of
Doctor of Philosophy
In the Department of Biological Sciences

Faculty of Science
University of Cape Town
January 2014
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The copyright of this thesis vests in the author. No
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quotation from it or information derived from it is to be

published without full acknowledgeement of the source.
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The thesis is to be used for private study or non-
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commercial research purposes only.

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Published by the Universit y of Cape Town (UCT) in terms
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of the non-exclusive license granted to UCT by the author.
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"Man is not an aquatic animal, but from the time we stand in youthful wonder
beside a spring brook till we sit in old age and watch the endless roll of the sea,
we feel a strong kinship with the waters of this world."
- Hal Borland (1964)

This thesis is dedicated to my loving parents Shirley and Trevor Ross-Gillespie
and to my wife Andrea Ross-Gillespie.
Declaration
PhD thesis title: Effects of water temperature on life-history traits of selected South African aquatic
insects: implications for the Ecological Reserve.

I, Vere Ross-Gillespie
Hereby

(a) grant the University of Cape Town free license to reproduce the above thesis in whole
or in part for the purpose of research;

(b) declare that:

(i) the above thesis is my own unaided work, both in concept and execution, and
that apart from the normal guidance from my supervisors, I have received no
assistance except as stated below:
Genetic sequencing was carried out by Dr. Tuuli Mäkinen of the South African Institute for Aquatic
Biodiversity in conjunction with the Canadian Centre for DNA Barcoding (CCDB) based at the
University of Guelph through the IDRC-IBOL project. GLM scripts for Matlab and R were written by
Andrea Ross-Gillespie.

(ii) neither the substance nor any part of the above thesis has been submitted in
the past, or is being, or is to be submitted for a degree at this university or at
any university.

I am now presenting the thesis for examination for the Degree of PhD
Signed:___________________________
Date:
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Table of Contents
Abstract ............................................................................................................................................... iv
Acknowledgements ............................................................................................................................. ix
1 General introduction and thesis overview ............................................................................ 1
1.1 Importance of lotic freshwater ecosystems ................................................................................ 2
1.2 Factors effecting the integrity of lotic freshwater ecosystems ................................................... 3
1.3 Balancing conservation and human resource use: the Ecological Reserve ................................ 8
1.4 A South African perspective .................................................................................................... 10
1.5 Research aims .......................................................................................................................... 11
1.6 Chapter outline ......................................................................................................................... 12
2 Site selection and site characteristics: selecting hydrological and thermal regime
gradients as a platform for life-history trait investigations ................................................ 14
2.1 Introduction .............................................................................................................................. 16
2.2 Methods .................................................................................................................................... 19
2.3 Results ...................................................................................................................................... 29
2.4 Discussion ................................................................................................................................ 45
3 Molecular investigations of Lestagella penicillata, Aphanicercella spp. and Chimarra
ambulans: genetic profiles for interpreting life-history traits ............................................ 52
3.1 Introduction .............................................................................................................................. 55
3.2 Methods .................................................................................................................................... 58
3.3 Results ...................................................................................................................................... 62
3.4 Discussion ................................................................................................................................ 71
4 Environmental modulation of life-history patterns ............................................................ 78
4.1 Introduction .............................................................................................................................. 81
4.2 Methods .................................................................................................................................... 84
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4.3 Results ...................................................................................................................................... 93
4.4 Discussion ............................................................................................................................. 113
5 The role of temperature in egg development .................................................................... 130
5.1 Introduction ........................................................................................................................... 132
5.2 Methods ................................................................................................................................. 134
5.3 Results ................................................................................................................................... 140
5.4 Discussion ............................................................................................................................. 153
6 The role of temperature in larval growth rates, survival and adult emergence of
Lestagella penicillata............................................................................................................ 169
6.1 Introduction ........................................................................................................................... 172
6.2 Methods ................................................................................................................................. 174
6.3 Results ................................................................................................................................... 181
6.4 Discussion ............................................................................................................................. 192
7 General discussion and synthesis ....................................................................................... 200
7.1 The evolution of life-histories ............................................................................................... 203
7.2 So what do the taxa in this study reveal ................................................................................ 208
7.3 The impact of climate change on life-histories and adaptive management mitigation ......... 217
7.4 Proposals for addressing current research lacunae ................................................................ 221
References ...................................................................................................................................... 224
Appendices ..................................................................................................................................... 256

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Abstract
Life-history studies have informed all areas of aquatic ecological research, whilst also providing
information relevant for conservation and management of aquatic systems. Given the large research gap
that has existed in this regard for Southern Hemisphere lotic systems, there has been an urgent need to
gather such data if effective management policies are to be implemented regionally, especially in the
face of ongoing development, anthropogenic impacts, and global climate change. Furthermore, there
has been a growing awareness of the need to incorporate thermal guidelines into legislation regarding
environmental flows and associated water management plans. In South Africa radical new legislation
introduced in 1996 resulted in rivers and aquatic ecosystems being given a right to water of their own-
essentially environmental flows, required to protect the aquatic ecosystems associated with the water
resource, that are determined separately for all or part of any significant water resource. This water,
including both the quantity and quality, is referred to as the “Ecological Reserve.” Baseline information
on the relationship between temperature and life-history patterns of aquatic insects is required to inform
the incorporation of thermal guidelines in the Ecological Reserve determination process.
Assuming such information can be gathered, a problem arises as to how the data can be interpreted and
incorporated into management guidelines. For instance if representatives of widespread species
occurring throughout a country are collected from a single location (say perhaps a single province in
South Africa) and then analysed in terms of their thermal limits for growth – would these limits hold
true for that same species where it occurs elsewhere? Intraspecific variability, cryptic species and
broader phylogenetic constraints all influence the thermal limits of species and need to be considered
when examining thermal influences on life-history patterns.
This thesis aimed to test the overarching hypothesis that while the life-history traits of aquatic insects
could be constrained to some degree by their evolutionary history, they would also be impacted by
thermal and hydrological regimes, inducing a degree of plasticity in their life cycles. This hypothesis
was tested by examining the key life-history traits of three representative taxa of aquatic insect, namely
Lestagella penicillata (Ephemeroptera), Aphanicercella spp. (Plecoptera) and Chimarra ambulans
(Trichoptera), and how they are driven by environmental and genetic factors in six rivers situated in the
south-western Cape Province of South Africa. More specifically the objectives of the thesis were to:
1. Select six study rivers that exhibit a range of environmental variability that could invoke life-
history plasticity in the same widespread aquatic insect species that inhabit them. Furthermore,
to investigate the interaction between flow, temperature and physicochemical variables in these
selected rivers and characterise specifically their thermal and hydrological characteristics.
2. Gauge the potential effects of changes to/and variability within hydrological and thermal
regimes on aquatic insects commonly used in bioassessment methods (SASS) and used as
bioindicators (EPT taxa) that inhabit these six selected study rivers. This would be achieved
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through the monthly collection and assessment of fundamental life-history data of the same
target species occurring at each of the sites (for the period of a year), which might reveal
evidence of phenotypically plastic responses (e.g. changes in voltinism and timing).
3. Gain further insight into lethal and sublethal effects of temperature on these organisms,
specifically in terms of upper and lower thermal limits for egg development, time requirement
for egg development, and percentage hatch success through laboratory experiments which aid
the interpretation of field-collected data. Furthermore to assess nymphal growth rates, upper
Lethal Temperature (LT ) mortality, and timing of emergence in individuals of the same
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species but from different localities reared under the same laboratory conditions to test if less
obvious phenotypically plastic responses are evident (e.g. differences in LT limits or growth
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rates)
4. Use genetic analyses to evaluate genetic divergence among the subpopulations of the selected
species in order to differentiate between phenotypic plasticity and genetic determinism as the
basis of life-history responses of the target aquatic species from different study sites.
5. Use these data to contribute towards the establishment of thermal guidelines for the Ecological
Reserve which address the relationship between temperature and life-histoty patterns, in order
to inform management of riverscapes in South Africa.
Rivers selected for the study showed range of hydrological variability, from a stable/constant and
predictable hydrological regime to an unpredictable and seasonally fluctuating hydrological regime
(Chapter 2). Temperature data collected during the biological sampling period revealed that the thermal
regime indeed correlated well to the hydrological regime of each site –sites that exhibited more stable
hydrological regimes also exhibited more stable thermal regimes. Site characterisation showed that sites
differed largely in terms of the magnitude, frequency, timing and duration of the thermal and
hydrological regimes but were similar in physicochemical properties. In turn this provided a suitable
gradient against which to compare life-history traits of selected aquatic insects.
Results of the molecular investigation, using the CO1 gene from target species collected from each of
the study sites, presented a prime example of a case where current taxonomy had overlooked cryptic
species diversity (Chapter 3). More specifically the data suggested that both L. penicillata (maximum of
28.7% CO1 gene divergence among the six study sites and the Table Mountain site) and C. ambulans
(maximum of 13.5% CO1 gene divergence between Table Mountain site compared to six study sites)
populations showed evidence of having diverged to the point where they could be considered to be
separate (sibling) species. For Aphanicercella, the CO1 gene was able to successfully resolve the four
species identified by current taxonomy. The presence of previously undescribed morphologically
cryptic species complexes, evolving under different environmental conditions (hydrological, thermal
and chemical) at the sites, could account for the divergences observed. However, the effects of
incomplete lineage sorting should not be ruled out. The presence of these species complexes could
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substantially confound results of life-history studies and experiments of species thermal tolerance
limits. In other words, variable egg development responses might be expected for L. penicillata
populations given knowledge of the evolutionary status of the different populations.
Monthly sampling of invertebrates was carried out for the period April 2009-April 2010 in the six rivers
within the Western Cape, during which target organisms collected each month were sorted, counted and
measured for life-history analyses (Chapter 4). Differences in the thermal and hydrological regimes
among the sites were found to indeed modulate life-history traits, where the same species was
concerned, and this was more noticeable in C. ambulans. This species exhibited less phylogenetic
constraint and more flexibility in terms of its life-history compared to L. penicillata and Aphanicercella
spp. which showed greater phylogenetic constraint and greater adaptation to site-specific conditions –
congruent with molecular analyses that showed higher genetic divergence among sites. Voltinism was
determined in each of the target taxa: L. penicillata and Aphanicercella spp. both exhibited a slow,
seasonal univoltine cycle with a single cohort easily tracked throughout the year, while C. ambulans
showed a non-seasonal or asynchronous multivoltine life cycle with multiple generations occurring
simultaneously. C. ambulans appeared to show a phenotypically plastic response to temperature, in that
more generations (trivoltinism) were observed in warmer rivers, in comparison to univoltine
populations in colder rivers. Optimal thermal ranges for growth were established through the use of
GLMs, and were found to be 13-21.5°C for L. penicillata, <11.5°C-14.5°C for Aphanicercella spp.,and
14.3°C- >21.5°C for C. ambulans). Overall, the life-history responses of the target species assessed in
this study appeared to be finely tuned to the hydrological and thermal regimes of each river studied.
This could have been as a result of site specific evolution and adaptation, perhaps showing similarities
on a catchment scale. However, where the same species showed differences in life-history responses
(number and duration of generations) amongst rivers, the data appeared to suggest that water
temperature was the most likely factor for these differences. The hydrological regime, on the other
hand, was found to be the major driver in determining population size and mortality while possibly
imposing a developmental time constraint for life-histories of the study taxa (especially C. ambulans
and Aphanicercella spp.). The possibility that the putative effects of discharge on life-cycle and
emergence might reflect synchronicity with the availability of key basal resources, or the effects of
seasonal conditions on adult fitness, could however not be discounted and would require further
investigation.
In order to better interpret field-collected life-history data (in terms of egg development duration,
potential diapause and confirmation of size-class of first-instar nymphs), experiments investigating egg
development across a range of water temperatures (5-30°C in 5°C intervals) were carried out in a
controlled environment in the laboratory for each of the target taxa (Chapter 5). Water temperature
effected the development of eggs of three genera quite differently. Experiments revealed that successful
egg development and hatching occurred between 10-20°C for L. penicillata, with a high percentage
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