Bottom-up effects via heterotrophic pathways in invertebrate assemblages of tropical streams: nutrients, leaf litter and the relationship between productivity and diversity

Connolly, Niall Michael (2016) Bottom-up effects via heterotrophic pathways in invertebrate assemblages of tropical streams: nutrients, leaf litter and the relationship between productivity and diversity. PhD thesis, James Cook University.

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Abstract

This project was instigated by the need to understand anthropogenic impacts on streams in the Queensland Wet Tropics bioregion, in particular the clearing of riparian vegetation and the increased flux of nutrients entering streams due to altered land use. Chapter 2 provides an introduction to the patterns and processes determining invertebrate diversity in streams in the Wet Tropics, and subsequent chapters describe how land-use change has altered the basal resources of these streams and how these changes influenced biological processes and their productivity and diversity. Nutrient enrichment interacts with the availability of organic matter and can reduce constraints on material flow and lead to increased productivity of invertebrates in these heterotrophic ecosystems. To understand these bottom-up influences I measured the response of invertebrate assemblages to two key basal resources – nutrients and terrestrial leaf litter – in manipulative experiments and in situ in streams subject to the impacts of agriculture.

I used artificial stream channels to investigate the effects of nutrient supplements on primary production, the decomposition of leaf litter, and the abundance and composition of the benthic invertebrate assemblage. In the first series of experiments the rates of decomposition were measured for leaves of four rainforest species with and without a broad nutrient supplement and with and without the presence of the shredder Anisocentropus kirramus. The decomposition of some leaf species was enhanced, but levels of chlorophyll a and fine particulate organic matter did not differ between treatment and control channels. Treatment channels contained 75% more invertebrates than control channels but only five of the total of 109 invertebrate species showed significant change (all positive), and there was no change in species richness or evenness. I also tested the effect of nitrogen and phosphorus nutrient enrichment separately. I measured the amount of leaf material consumed or decomposed and the microbial biomass colonising the leaves. Supplements of phosphorus, but not nitrogen, enhanced leaf breakdown, microbial growth and growth of A. kirramus larvae. Microbial biomass and dry mass of larvae increased with nutrient enrichment and they were significantly correlated. Thus the phosphorus supplement was transmitted through the detrital food web via the microbial pathway, resulting in higher nutritional quality of leaves and enhanced physiological condition of the shredder.

The lack of a response in the assemblage composition to nutrient enrichment was surprising given the magnitude of the nutrient enhancement and because it was clearly entering trophic pathways. To investigate the relationship between productivity and diversity, and how it might apply in these heterotrophic stream assemblages, I tested how the availability of a major resource (the abundance of leaf litter) affected invertebrate productivity and diversity at two scales (individual cobble/leaf packs in artificial stream channels, and whole-channel scales) and investigated the mechanisms by which different patterns, positive or negative, and particularly a hump-shaped relationship between productivity and diversity, could be explained. At the channel scale, macroinvertebrate diversity increased monotonically with the number of leaf packs present in the channels. However, at the cobble/leaf-pack scale, diversity had a humpshaped relationship with % leaf pack cover.

The divergence between channel-scale and cobble/leaf-pack-scale richness at high % leaf-pack cover suggested that there were new species occurring in cobble/leaf packs in the treatment with higher % leaf-pack cover. In contrast with prevailing theory, β diversity was consistently high and the monotonic increase in invertebrate richness was attributed to the increasing number of individual cobble/leaf packs in the higher-cover treatments. That is, despite a unimodal pattern at the smaller scale, the monotonic pattern at the larger scale was due to high β diversity ensuring a strong species-area effect.

I measured the rates of colonisation and dispersal of invertebrates on leaf litter packs to confirm the duration of experiments and test the concept that immigration limitation was responsible for the hump-shaped productivity-diversity relationship at small scales. I tracked the composition of the invertebrates colonising leaf packs through time and fitted an equilibrium model to the data to provide estimates of immigration and emigration rates. Emigration rates were also independently determined using drift nets. Both the mean number of individuals and mean number of taxa systematically approached an upper limit by day 24 although turnover of taxa on leaf packs continued to occur. A few taxa had very high mobility, with 50% or more individuals moving each day. Many other taxa had a pattern of slower, more sustained colonisation with less than 10% of individuals leaving a site each day. Ordination indicated a progressive shift in assemblage composition through the colonisation period and a convergence of the compositions on days 24 and 38. These results suggest that the invertebrate assemblage inhabiting the leaf packs approximated equilibrium and was in a dynamic flux at small (leaf pack) scales.

The numbers of potential invertebrate immigrants entering the artificial stream channels through drift was determined by the stream flow into the channels. Thus, differences in the number of leaf packs within the channels in the productivity gradient experiments altered the immigration probabilities at the cobble/leaf pack scale, and it was concluded that constrained immigration dynamics at high litter pack levels was responsible for the declining limb in the hump- shaped productivity-diversity pattern. These results are particularly interesting in that a hump-shaped pattern was nested within a monotonic pattern at the larger scale, even within a confined system, and provide new insight in to how a productivity gradient might affect diversity in biological communities and be scale-dependent.

To generalise the results of these experiments and test them in a large-scale environment, I investigated patterns of water quality and macroinvertebrate distributions in streams affected by agricultural land use. There was a strong negative relationship between invertebrate richness and distance downstream, driven by a gradient of reducing substratum particle size. The abundance of invertebrates was most strongly influenced by mean sediment size, while invertebrate richness was influenced by a combination of sediment size and the availability of coarse particulate organic matter (CPOM), mainly terrestrial leaf litter. When substratum particle size was accounted for, richness was reduced by ~24% in streams with limited availability of CPOM, resulting from lower riparian forest cover upstream. High concentrations of fertilizer-derived nitrate may have boosted invertebrate abundances, but only in upper-mid sections of streams, where coarse substrata (> 100 mm) and high insolation were available. My results indicated only a modest effect of the riparian zone on NOₓ–stripping compared with the large input from agricultural land use, and suggest that with current inputs, the NOₓ concentrations in these streams are largely independent of the riparian zone. The consistent pattern of downstream increase in NOₓ concentrations, and the short residence times of water in these streams, also suggests there is no major in-stream uptake of NOₓ. Therefore, it appears that the majority of inorganic nitrogen entering these streams from surrounding agriculture is not being utilised within the stream, but is exported.

Concentrations of different species of phosphorus showed little change or a decline in concentration with distance downstream. However, particulate and dissolved nitrogen and phosphorus concentrations did increase significantly following rainfall, indicating that both are exported from the catchment. The total phosphorus concentrations in these streams were similar to, or above, the response concentrations observed in the enrichment experiments (~20 μgP L⁻¹), but concentrations of filterable reactive phosphorus (FRP) were generally lower than those that induced a response in the experiments. The low concentrations of FRP and the decline in concentration with distance downstream suggest that phosphorus was being assimilated and, particularly given the abundance of NOₓ, it appears likely that phosphorus is limiting in these streams. This concurs with the findings of the enrichment experiments, and may explain the weak response of the invertebrate assemblage to the greatly increased NOₓ concentrations in the streams.

The components of this thesis enhance understanding of how selected human impacts affect the ecology of the invertebrate assemblages of low-order streams in the Wet Tropics bioregion. I have demonstrated how organic matter and nutrient availability play a central role in the ecology of these streams and how the strong linkages between nutrient and carbon cycles influence decomposer activity, consumer nutrition and energy flow through their food webs. I have also demonstrated responses of invertebrate assemblages to land-use impacts and, more importantly, I have explained the mechanisms by which the ecology and biodiversity of these systems have been modified by shifts in the basal resources, productivity and transfer of energy and nutrients. It is important to understand the processes that determine the humpshaped productivity-diversity relationship because productivity is increasingly being affected by anthropogenic fertilisation in both terrestrial and aquatic environments. Therefore, an understanding of the processes that produce the hump-shaped relationship will help us to predict when a decline in diversity might occur and to develop the necessary measures to predict a decline in diversity.

Item ID: 46021
Item Type: Thesis (PhD)
Keywords: agricultural impact, biodiversity, community ecology, conservation, decomposition, diversity, endemic, groundwater, human impact, humus, indicators, invertebrates, leaf litter, macroinvertebrates, nitrate, nutrient pollution of water, nutrients, organic matter, organic water pollutants, pollution, productivity, Queensland, rainforest, riparian ecology, riparian, shredder, stream community, streams, sugarcane, tropical biology, tropical streams, tropics, Wet Tropics
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Additional Information:

Publications arising from this thesis are available from the Related URLs field. The publications are:

Chapter 2: Connolly, Niall M., Christidis, Faye, McKie, Brendan, Boyero, Luz, and Pearson, Richard (2008) Diversity of invertebrates in wet tropics streams: patterns and processes. In: Stork, Nigel E., and Turton, Stephen M., (eds.) Living in a Dynamic Tropical Forest Landscape. Blackwell Publishing, Carlton, VIC, Australia, pp. 161-177.

Chapter 2: Pearson, Richard G., Connolly, Niall M., and Boyero, Luz (2015) Ecology of streams in a biogeographic isolate— the Queensland Wet Tropics, Australia. Freshwater science, 34 (2). pp. 797-819.

Chapter 3: Pearson, R.G., and Connolly, N.M. (2000) Nutrient enhancement, food quality and community dynamics in a tropical rainforest stream. Freshwater Biology, 43 (1). pp. 31-42.

Chapter 3: Connolly, N.M., and Pearson, R.G. (2013) Nutrient enrichment of a heterotrophic stream alters leaf litter nutritional quality and shredder physiological condition via the microbial pathway. Hydrobiologia, 718 (1). pp. 85-92.

Chapter 6: Connolly, N.M., Pearson, R.G., Loong, D., Maughan, M., and Brodie, J. (2015) Water quality variation along streams with similar agricultural development but contrasting riparian vegetation. Agriculture, Ecosystems and Environment, 213. pp. 11-20.

Chapter 6: Connolly, Niall, Pearson, Richard, and Pearson, Benjamin (2016) Riparian vegetation and sediment gradients determine invertebrate diversity in streams draining an agricultural landscape. Agriculture, Ecosystems and Environment, 221. pp. 163-173.

Date Deposited: 11 Oct 2016 03:52
FoR Codes: 05 ENVIRONMENTAL SCIENCES > 0502 Environmental Science and Management > 050299 Environmental Science and Management not elsewhere classified @ 50%
06 BIOLOGICAL SCIENCES > 0602 Ecology > 060204 Freshwater Ecology @ 50%
SEO Codes: 96 ENVIRONMENT > 9605 Ecosystem Assessment and Management > 960506 Ecosystem Assessment and Management of Fresh, Ground and Surface Water Environments @ 25%
96 ENVIRONMENT > 9609 Land and Water Management > 960907 Forest and Woodlands Water Management @ 75%
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