The ecological role of mosquito larvae in aquatic environments

The ecological role of mosquito larvae in aquatic environments

The ecological role of mosquito larvae in aquatic environments

Assessing the community role and trophic interactions of Anopheles gambiae larvae in the Volta Region of Ghana.

IMAGE CREDIT: Michelle L. D’Souza

 The Anopheles gambiae mosquito complex, which consists of eight species, is the prevalent malaria vector in Sub-Saharan Africa1. While we have a reasonable understanding of predation rates, resource availability, and competition among aquatic invertebrate2-7, we lack a comprehensive appreciation of the larval ecology of An. gambiae, including their trophic role, diets, and population dynamics. My research aims to address this gap, crucial in integrating aquatic habitat management with vector control programs8.

With the advance of DNA technologies such as metabarcoding, we can now identify prey to a species level by examining the stomach contents of aquatic predators. When using these insights with network analyses, it is possible to quantify direct and indirect ecological interactions in the environment9. I will take advantage of these techniques for my research which aims to assess the trophic interactions of An. gambiae larvae in water bodies within two agricultural communities in Ghana.

I will collect mosquito larvae with a dipper, and a larger subset of invertebrates with an aquatic net (with a mesh size of 250 μm).  Each specimen’s gut contents will be analyzed using DNA barcoding and this data will be used to gain an understanding of the larval niche and ultimately An. gambiae’s role within the aquatic community. I will examine network interaction metrics such as connectance (the number of realized connections between species relative to what is available), degree (the number of interaction partners), betweenness (the importance of a species as a connector between different groups), and closeness (how central a focal species is in the community) to aid in niche construction. Temperature, pH, dissolved oxygen, salinity, and conductivity of the target water bodies will also be measured while sampling as these factors affect the occurrence and abundance of larvae by influencing the breeding behaviours of mosquitoes10.

In addition, I plan to study how different species of mosquito larvae compete for key resources. In the laboratory, the densities of local-caught larval populations of An. gambiae and other mosquito species will be manipulated to help determine the strongest competitor. While maintaining optimal rearing conditions by measuring the physio-chemical properties of the water daily, I will examine four indicators of overall growth and survival (the mean time to pupation, percentage of larvae that did not reach the adult stage, sex ratio, and mean female wing length) and therefore infer competitive strength among species. These data will provide important insights into predicting whether another mosquito species would dominate if the number of An. gambiae is reduced in the habitat.

An. gambiae is relatively small, constituting about half to one-third the mass of many Aedes mosquito species12. Foraging theory indicates that small, mobile insects of low profitability, do not form a preferred food source to predators unless they are massively clustered13. Though many species feed on mosquitos, these animals also feed on other small organisms that typically co-occur with An. gambiae14. For these reasons, I do not foresee that An. gambiae larvae will be a key food source for any predator in the aquatic environments in Ghana or that they will have a central role in local trophic systems.

If this is proven to be true, it will provide evidence that malaria-intervention methods that aim to suppress or reduce An. gambiae mosquitoes will not have detrimental consequences for the larger community.

Written by

Afia S. Karikari

Afia S. Karikari

African Regional Postgraduate Programme in Insect Science, University of Ghana, Accra, Ghana  

April 21, 2021

doi:10.21083/ibol.v11i1.6619 

This research is part of a larger effort by Target Malaria in Ghana to understand the role of the An. gambiae mosquito in the broader ecosystem.

For more information see:

The important interactions behind the itch

References:

  1. Service MW (1971) Studies on sampling larval populations of the Anopheles gambiae Bulletin of the World Health Organization 45:169–180.
  2. Service MW (1973) Mortalities of the larvae of the Anopheles gambiae Giles complex and detection of predators by the precipitin test. Bulletin of Entomological Research 62:359– 369.
  3. Service MW (1977) Mortalities of the immature stages of species of the Anopheles gambiae complex in Kenya: comparison between rice fields and temporary pools, identification of predators, and effects of insecticidal spraying. Journal of Medical Entomology 13:535–545.
  4. Ho BC, Ewert A, Chew LM (1989) Interspecific competition among Aedes Aegypti, albopictus and Ae. triseriatus (Diptera: Culicidae). Journal of Medical Entomology. 26:615–623.
  5. Barrera L (1996) Competition and resistance to starvation in larvae of container-inhabiting Aedes mosquitos. Ecological Entomology 21:117–127.
  6. Juliano SA, Lounibos LP and O’Meara GF (2004) A field test for competitive effects of Aedes albopictus on aegypti in south Florida: differences between sites and co-existence and exclusion? Oecologia. 139:583–593.
  7. Braks MAH, Honόrio NA, Lounibos LP, Lourenςo-de-Oliveira R, Juliano SA (2004) Interspecific competition between two invasive species of container mosquitos, Aedes aegypti and Aedes albopictus (Diptera: Culicidae), in Brazil. Annual Entomological Society of America 97:130–139.
  8. Li L, Bian L, Yakob L, Zhou U, Yan G (2009) Temporal and spatial stability of Anopheles gambiaelarval habitat distribution in western Kenya highlands. International Journal of Health Geographics. 8(70). doi:10.1186/1476-072X-8-70
  9. Fath BD, Patten BC (1998) Network synergism: emergence of positive relations in ecological systems. Ecological Modelling 107:127–143.
  10. Clements AN (1992) The Biology of Mosquitoes (Vol 1) Development, Nutrition and Reproduction. Chapman and Hall, London.
  11. Paajimans KP, Huijben S, Githeko AK, Takken W (2009) Competitive interactions between larvae of the malaria mosquitos, Anopheles arabiensis and Anopheles gambiae under semi-field conditions in western Kenya. Acta Tropica. 109:124–
  12. Koella JC, Lyimo EO (1996) Variability in the relationship between weight and wing length of Anopheles gambiae (Diptera: Culicidae). Journal of Medical Entomology 33: 261–264.
  13. Stephens DW, Brown JS, Ydenberg RC (2007) Foraging: Behavior and Ecology. University of Chicago Press, Chicago, IL.
  14. Findley JS, Black H (1983) Morphological and dietary structuring of a Zambian insectivorous bat community. Ecology 64:625–630.

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Judge a caterpillar by what they eat, not where they’re found

Judge a caterpillar by what they eat, not where they’re found

Judge a caterpillar by what they eat, not where they’re found

Gut content analysis of Peruvian caterpillars reveals new insights into host-plant relationships and the methods used to examine species interactions key to BIOSCAN

The original primary rainforest surrounding Panguana station, Peru, Dept Huánuco, western Amazonia.

PHOTO CREDIT: K. Wothe

Understanding species and their associations with each other and with the environment – a key aspect of synecological research – is of great importance. For example, data on insect-host plant relationships can aid investigations into food webs and extrapolations of global species numbers as well as inform forestry, agriculture, and conservation practices.

Supported by the Bavarian Ministry of Science (‘SNSB-Innovativ’), our recent pilot study examined the gut contents of Peruvian caterpillars demonstrating the potential for gathering large-scale data on species interactions when applying DNA barcoding and high-throughput sequencing technologies. We obtained 130 caterpillars (moth larvae) by canopy fogging at the Panguana research station, an area of tropical primary forest in western Amazonia. DNA barcode analysis resulted in 119 successfully sequenced larvae, more than half of which matched with moth reference sequences on BOLD. Surprisingly high biodiversity was uncovered from our modest sample – 92 BINs or species proxies. The trees from which caterpillars were collected were also identified, both by morphology and DNA barcoding.

Panguana research station, Peru, Dept Huánuco, western Amazonia, with the characteristic Lupuna tree (Ceiba pentandra, Malvaceae) in the background.

PHOTO CREDIT: J. Diller

Knowing the tree and larva identity is not enough to conclude a host-plant relationship, particularly in a dense tropical rainforest. Caterpillars may in fact be feeding on the epiphytes, lianas, lichens, algae, fungi, or mosses associated with trees (i.e., alternative feeding), and sometimes larvae may have been fogged down from neighbouring trees. To confirm a direct insect-host plant relationship, we partnered with the company Advanced Identification Methods (AIM) to design a high-throughput sequencing (HTS) protocol with plant markers (rbcL, psbA) that would enable the identification of plant matter from the gut contents of ten larvae. Results revealed only two matches between the fogged tree and larval gut content which suggests a rather high percentage of alternative feeding. In three cases, the gut content clearly indicated feeding on lianas and neighbouring trees. Interestingly, the analysis of four larvae resulted in the putative presence of Bryophyta, suggesting moss-feeding in Lepidoptera, a phenomenon rarely observed. Potential contamination (for example, through the diffusion of plant DNA into the alcohol of the bulk sample) has yet to be ruled out, work which is currently being validated in a subsequent project investigating the gut contents of an additional 190 larvae.

Automeris denticulata (Conte, 1906) (Saturniidae): Larva (left), selected from canopy fogging bulk samples of a Poulsenia (Moraceae) tree at the Panguana station, identified by its COI barcode; Adult (right), collected at the Panguana station.

PHOTO CREDIT: Mei-Yu Chen & Dr. R. Mörtter

Our approach of combined canopy fogging, DNA-based identification, and gut content analysis resulted in two key findings. First, a significant portion of both insect and plant taxa can be identified even in highly diverse, tropical regions – more than 97% to a family level and about 80% to a species or genus level. Secondly, we can successfully confirm or reject the hypothesis that caterpillars feed on the trees where they are collected by identifying their diets through an HTS protocol on gut contents. Importantly, the taxonomic resolution of animal and plant identifications will increase with further investments into DNA reference libraries. We recommend specimen de-contamination (e.g. by bleaching) and/or isolated storage of the target taxa rather than bulk storage to improve the reliability of gut content analysis.

Urania leilus (Linnaeus, 1758) (Uraniidae): Larva (left), selected from canopy fogging bulk samples of an Oxandra polyantha (Annonaceae) tree at the Panguana station, identified by its COI barcode; Adult (right).

PHOTO CREDIT: Mei-Yu Chen & Dr. J. Diller

The techniques employed in our pilot have immense potential for unveiling trophic interactions in tropical regions at a very large scale as they are fast and cost-effective. The latter is enabled, in part, by the availability of target specimens in the by-catch of other studies. For example, our efforts fogging 150 trees in a separate project assessing the biodiversity of ants have resulted in 1,200 lepidopteran larvae. Subsequent aspects of the workflow, from selecting the larvae from bulk samples, tissue sampling, photography, and databasing, required 10–20 minutes per larva and can be performed with relatively low expertise. The costs for subsequent lab work, i.e. identification of larvae and their gut contents, currently amount to 20–25 € per larva and these costs will soon drop considerably. In contrast, traditional approaches involving the searching and rearing of larvae, and the identification of hatched adults by experts is massively time and resource consuming.

Providing reliable data on trophic interactions is one of the major goals of the BIOSCAN program, one that will be a powerful tool for investigating food webs, for determining the amplitude of alternative or multiple feeding sources, and for the study of phagism (monophagy versus polyphagy), thus gaining data for extrapolations of global species numbers. These data will also be particularly important for pest management in forestry, and agriculture, and for conservation purposes.

Overcoming the current lack of knowledge is a major challenge, particularly in ecoregions with megadiverse faunas and floras. Yet, its success is imperative for humanity considering the unprecedented biodiversity losses we currently face. In this context, the recently launched BIOSCAN with its focus on revealing species interactions will embolden an important plan for the international research community to come together in understanding nature and conserving it for a sustainable future.

 

Read the complete manuscript in PLoS ONE.

Written by

Axel Hausmann

Axel Hausmann

Juliane Diller

Juliane Diller

Amelie Höcherl

Amelie Höcherl

SNSB – Staatliche Naturwissenschaftliche Sammlungen Bayerns - Zoologische Staatssammlung München, Munich, Germany

May 6, 2020
https://doi.org/10.21083/ibol.v10i1.6133 

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