Table Of ContentDirk Weihrauch
Michael O’Donnell
Editors
Acid-Base Balance
and Nitrogen
Excretion in
Invertebrates
Mechanisms and Strategies
in Various Invertebrate Groups
with Considerations of Challenges
Caused by Ocean Acidifi cation
Acid-Base Balance and Nitrogen Excretion in Invertebrates
Dirk Weihrauch • Michael O’Donnell
Editors
Acid-Base Balance
and Nitrogen
Excretion in
Invertebrates
Mechanisms and Strategies in Various Invertebrate Groups with
Considerations of Challenges Caused by Ocean Acidification
Editors
Dirk Weihrauch Michael O’Donnell
University of Manitoba Department of Biology
Winnipeg McMaster University
Manitoba Hamilton
Canada Ontario
Canada
ISBN 978-3-319-39615-6 ISBN 978-3-319-39617-0 (eBook)
DOI 10.1007/978-3-319-39617-0
Library of Congress Control Number: 2016959038
© Springer International Publishing Switzerland 2017
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V
Preface
The Importance of Invertebrates
Invertebrates rule the world in terms of number of species, number of individuals, and
biomass. Over 95 % of species are invertebrates, and this diversity may be a consequence
of the small size of most invertebrates (Wilson 1987). Their niches are thus also small, so
the environment can be divided into multiple domains in which specialists can coexist.
Biodiversity may also follow from their greater antiquity, in that invertebrates have had
more time for exploration of the environment and evolution of specialist traits. Inverte-
brates are also the most common animals in terms of number of individuals; copepods
and nematodes are the most common multicellular animals in marine and terrestrial
environments, respectively. Invertebrates also rule the earth in terms of body mass; a typ-
ical hectare of Brazilian rain forest may contain 200 kg dry weight of animal body tissue,
of which 93 % consists of invertebrates. Recent estimates suggest that the world holds 1018
insects, equivalent to more than 200 million insects for each human on the planet and 300
pounds of insects for every pound of humans. Their numbers and biomass have important
implications for the earth’s ecosystems. For example, the principal consumers of vegeta-
tion in Central and South America are not deer, rodents, or birds, but leaf-cutter ants.
Invertebrates also play dominant roles in ecosystem services, which are the benefits pro-
vided by ecosystems for humankind and which include supporting, provisioning, and
regulating services (Prather et al. 2013). Invertebrates provide supporting services for pri-
mary production directly through pollination and seed dispersal and indirectly through
a cascades and nutrient cycling. Insect pollination is required for ~75 % of all the world’s
food crops and is estimated to be worth ~10 % of the economic value of the world’s entire
food supply. Globally, pollinators appear to be strongly declining in both abundance and
diversity. The loss of pollinator species may result in reduced seed set, reduced fitness, and
lower population viability of flowering plants. Most primary production eventually enters
detrital food webs in which the dominant consumers and nutrient cyclers are inverte-
brates. Soil invertebrates break down soil organic matter and recycle nutrients in terres-
trial ecosystems. Earthworms, for example, burrow and facilitate water flow and storage,
soil aeration, and root development. As a consequence, changes in the decomposer fauna
alter the physical and chemical environment, with consequent “bottom-up” effects on
primary producers and higher trophic levels. Reef-building corals also provide support-
ing services by producing structures that serve as habitat for most coastal fish species.
Provisioning services refer to goods obtained from ecosystems and include food, natural
products, and pharmaceuticals obtained from insects, shrimp, crabs, scallops, oysters,
lobsters, corals, sea cucumbers, and many others.
Regulating services are those that regulate ecosystem processes or maintain ecosystem
structure. Invertebrates have important impacts on water quality, stabilization of food
webs, and regulation of diseases and pests or invasive species. In shallow water, bivalves
(i.e., mussels and oysters) may filter 10–100 % of the water column; in the case of the
invasive zebra mussel (Dreissena polymorpha) in the Great Lakes, excessive water filtra-
tion has reduced plankton levels and thus altered food webs. Invertebrates are important
not only as hosts for parasites and pathogens but also as predators and p arasitoids that
regulate many parasites and disease vectors. Human diseases transmitted by invertebrate
V I Preface
vectors include malaria, dengue, onchocerciasis, and Lyme disease. Schistosomes and
nematodes may cause disease directly. On the other hand, invertebrates play important
roles in biocontrol of crop-feeding insects and disease vectors through parasitism, direct
predation, or transmission of viruses, bacteria, and toxins.
For scientific, economic, and ethical reasons, invertebrates also play increasingly impor-
tant roles as model organisms in fields such as genetics, developmental biology, toxicol-
ogy, and physiology. Insects (Drosophila), nematodes (C. elegans), and protozoans
(Tetrahymena) have long been used in studies of genetics and developmental biology.
The flatworm Schmidtea mediterranea has been useful in studies of regeneration, and the
crustacean Daphnia is widely used in studies of toxicology.
This book had its genesis, in part, on the authors’ concerns that anthropogenic activities,
especially the increasing levels of carbon dioxide in the earth’s atmosphere resulting
from the burning of fossil fuels, pose enormous challenges for most species. In particu-
lar, the loss of species abundance and diversity is troubling. For invertebrates, 67 % of
monitored populations show a 45 % decline in mean abundance (Dirzo et al. 2014). For
aquatic organisms, reductions in water pH as a consequence of elevations in ambient
carbon dioxide levels create challenges on shell deposition in crustaceans, mollusks, and
corals. However, the lower pH may facilitate the elimination of ammonium as a nitrog-
enous waste. Too much nitrogen in soils following application of fertilizer may lead to
depletion of other important minerals such as calcium, phosphorus, and magnesium.
Nitrogen-polluted air, resulting from release of nitrates from automobiles and industrial
plants, also results in this acidification of the soil when acid rain falls.
This book summarizes therefore the most current views on acid–base homeostasis and
nitrogen excretion strategies as well as the effects of increasing environmental CO levels in
2
a broad range of phyla and subphyla, including reef-building cnidarians, planarians, nem-
atodes, leeches, echinoderms, aquatic and terrestrial crustaceans, cephalopods, and insects.
The book also describes regulatory mechanisms in key species like Caenorhabditis elegans
(genetic model system), Schmidtea mediterranea (regenerative model system), Strongylo-
centrotus droebachiensis (developmental model system), Carcinus maenas (physiologic
model system, aggressive invasive species), Sepioteuthis lessoniana (commercially relevant
cephalopod), and Aedes aegypti and Rhodnius prolixus (disease vectors). Additionally, a
chapter is dedicated to elaborate on the physiological importance of the Na+/K+-ATPase,
which is essential for ammonia excretion and acid–base regulatory processes.
Dirk Weihrauch
Winnipeg, MA, Canada
Michael O’Donnell
Hamilton, ON, Canada
References
Dirzo R, Young HS, Galetti M, Ceballos G, Isaac NJ, Collen B (2014) Defaunation in the Anthropocene. Sci-
ence 345(6195):401–406
Prather CM, Pelini SL, Laws A, Rivest E, Woltz M, Bloch CP, Del Toro I, Ho CK, Kominoski J, Newbold T
(2013) Invertebrates, ecosystem services and climate change. Biol Rev 88(2):327–348
Wilson EO (1987) The little things that run the world (the importance and conservation of invertebrates).
Conser Biol 1:344–346
VII
Contents
1 Nitrogen Excretion in Aquatic Crustaceans .............................................................. 1
Dirk Weihrauch, Sandra Fehsenfeld, and Alex Quijada-Rodriguez
2 Nitrogenous Waste Metabolism Within Terrestrial Crustacea,
with Special Reference to Purine Deposits and Their Metabolism ................... 25
Stuart M. Linton, Jonathan C. Wright, and Caitlin G. Howe
3 Gill Ion Transport ATPases and Ammonia Excretion in Aquatic
Crustaceans ............................................................................................................................................ 61
Francisco A. Leone, Malson N. Lucena, Daniela P. Garçon,
Marcelo R. Pinto, and John C. McNamara
4 Nitrogen Excretion and Metabolism in Insects .............................................................. 109
M. J. O’Donnell and Andrew Donini
5 Nitrogen Excretion in Nematodes, Platyhelminthes, and Annelids ................. 127
Alex R. Quijada-Rodriguez, Aida Adlimoghaddam,
and Dirk Weihrauch
6 Acid–Base Regulation in Aquatic Decapod Crustaceans ......................................... 151
Sandra Fehsenfeld and Dirk Weihrauch
7 Cell Biology of Reef-Building Corals: Ion Transport,
Acid/Base Regulation, and Energy Metabolism ............................................................ 193
Martin Tresguerres, Katie L. Barott, Megan E. Barron,
Dimitri D. Deheyn, David I. Kline, and Lauren B. Linsmayer
8 Acid–Base Regulation in Insect Haemolymph ................................................................ 219
Philip G.D. Matthews
9 Acid–Base Loops in Insect Larvae with Extremely Alkaline
Midgut Regions ................................................................................................................................... 239
Horst Onken and David F. Moffett
10 pH Regulation and Excretion in Echinoderms ................................................................ 261
Meike Stumpp and Marian Y. Hu
11 Acid–Base Regulation and Ammonia Excretion in Cephalopods:
An Ontogenetic Overview ............................................................................................................ 275
Marian Hu and Yung-Che Tseng
Service Part
Index ........................................................................................................................................................... 301
IX
Contributors
Aida Adlimoghaddam Department of Biological Sciences, University of Manitoba,
Winnipeg, MB, Canada
Katie L. Barott Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Megan E. Barron Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Dimitri D. Deheyn Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Andrew Donini Department of Biology, York University, Toronto, ON, Canada
Sandra Fehsenfeld Department of Zoology, University of British Columbia,
Vancouver, BC, Canada
Daniela P. Garçon Universidade Federal do Triângulo Mineiro, Campus de Iturama,
Iturama, MG, Brazil
Caitlin G. Howe Department of Environmental Health Sciences,
Mailman School of Public Health, Columbia University, New York, NY, USA
Marian Y. Hu Institute of Physiology, Christian-Albrechts-University of Kiel,
Kiel, Germany
David I. Kline Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Smithsonian Tropical Research Institute, Balboa, Panama
Francisco A. Leone Departamento de Química, Ciências e Letras de Ribeirão Preto,
Universidade de São Paulo, Ribeirao Preto, Sao Paulo, Brazil
Lauren B. Linsmayer Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Stuart M. Linton School of Life and Environmental Sciences, Deakin University,
Waurn Ponds, VIC, Australia
Malson N. Lucena Departamento de Química, Ciências e Letras de Ribeirão Preto,
Universidade de São Paulo, Ribeirão Preto, Ribeirao Preto, Sao Paulo, Brazil
Philip G.D. Matthews Department of Zoology, University of British Columbia,
Vancouver, BC, Canada
John C. McNamara Departamento de Biologia, Faculdade de Filosofia,
Ciências e Letras de Ribeirão Preto, Universidade de São Paulo, Ribeirão Preto,
Sao Paulo, Brazil
Centro de Biologia Marinha, Universidade de São Paulo, Ribeirão Preto,
Sao Paulo, Brazil
X Contributors
David F. Moffett School of Biological Sciences, Washington State University,
Pullman, WA, USA
M.J. O’Donnell Department of Biology, McMaster University, Hamilton, ON, Canada
Horst Onken Department of Biological Sciences, Wagner College, Staten Island,
NY, USA
Marcelo R. Pinto Departamento de Química, Ciências e Letras de Ribeirão Preto,
Universidade de São Paulo, Ribeirão Preto, Ribeirão Preto, Sao Paulo, Brazil
Alex R. Quijada-Rodriguez Department of Biological Sciences,
University of Manitoba, Winnipeg, MB, Canada
Meike Stumpp Department of Zoophysiology, Zoological Institute at
Christian-Albrechts-University Kiel, Kiel, Germany
Martin Tresguerres Scripps Institution of Oceanography, University of California
San Diego, La Jolla, CA, USA
Yung-Che Tseng Marine Research Station, Institute of Cellular and Organismic
Biology, Academia Sinica, Taipei, Taiwan
Dirk Weihrauch Department of Biological Sciences, Institute of Cellular and
Organismic Biology, Academia Sinica, Taipei, Taiwan
Jonathan C. Wright Department of Biology, Pomona College, Claremont, CA, USA
1
1
Nitrogen Excretion
in Aquatic Crustaceans
Dirk Weihrauch, Sandra Fehsenfeld, and Alex Quijada-Rodriguez
1.1 Summary – 2
1.2 Introduction – 2
1.2.1 Synthesis of Nitrogenous Waste Products
in Aquatic Crustaceans – 2
1.2.2 Toxicity of Ammonia in Crustaceans – 3
1.2.3 Habitat and Physiological Adaptations – 5
1.2.4 Hemolymph Ammonia and Urea Concentrations
in Aquatic Crustaceans – 6
1.3 Tissues Involved in the Excretion
of Nitrogenous Waste Products – 6
1.3.1 Excretion Rates of Ammonia and Urea
in Aquatic Crustaceans – 6
1.3.2 Antennal/Maxillary Glands – 6
1.3.3 Gills – 8
1.4 Branchial Ammonia Excretion – 9
1.4.1 Capacity of Active Ammonia Excretion
in Gills of Different Haline Crab Species – 9
1.4.2 Mechanism of Branchial Ammonia Excretion
in Decapod Crabs – 10
1.5 Conclusion and Summarizing Working Model
of Branchial Ammonia Excretion Proposed
for the Green Shore Crab Carcinus maenas – 20
R eferences – 21
© Springer International Publishing Switzerland 2017
D. Weihrauch, M. O’Donnell (eds.), Acid-Base Balance and Nitrogen Excretion in Invertebrates,
DOI 10.1007/978-3-319-39617-0_1