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PHYSIOLOGY OF THE CLADOCERA
This page intentionally left blank
PHYSIOLOGY
OF THE
CLADOCERA
SECOND EDITION
Nikolai N. Smirnov
A. N. Severtsov Institute of Ecology and Evolution, Russian Academy of Sciences, Moscow, Russia

With Additional Contributions

Academic Press is an imprint of Elsevier
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 Contents

List of Contributors ix 5.4 Hemoglobin and Iron 93

5.5 Evolution of Carbon Dioxide and the Respiratory
Preface xi Quotient (RQ) 96
Acknowledgments xiii 5.6 Energy Budget 97
Abbreviations and Units xv 5.7 Hypoxia 97
5.8 Anoxia 99
1. General 5.9 Impact of Xenobiotics on Respiration 100

1.1 Systematic Position 1 6. Circulation

1.2 General Morphological Background 1
1.3 Geographic Distribution 6 6.1 Anatomical Background 101
1.4 Species-Specific Effect of Xenobiotics 7 6.2 Blood Flow 102
6.3 Heart Rate 103
2. Methods 6.4 Heart Regulation 106
6.5 Heart Arrest 109
2.1 Methods of Collection 9 6.6 Adhesion of Blood Cells 110
2.2 Observation of Living Specimens 9 6.7 Phagocytosis 110
2.3 Cultivation 9 6.8 Impact of Xenobiotics on Heart Rate 111
2.4 Immobilization and Attaching 10
2.5 Microscopy 11 7. Excretion
2.6 Biochemical and Special Physiological Methods 11
7.1 Anatomical Background 113
3. Chemical Composition 7.2 The Process of Excretion 114
7.3 Bioaccumulation of Toxic Substances 116
3.1 Lability of Chemical Composition 13 7.4 Transformation of Xenobiotics 118
3.2 Moisture Content and Calorific Value 13 7.5 The Routes of Elimination of Xenobiotics 118
3.3 Principal Constituents 13
3.4 Accumulation of Xenobiotics in the Cladoceran 8. Osmotic Regulation
Body 36
8.1 Potential Anatomical Background 121
4. Nutrition 8.2 Environmental Background 121
8.3 Water Balance 122
4.1 Feeding 39 8.4 Process of Osmotic Regulation 123
4.2 Digestion 60 8.5 Effect of Xenobiotics on Osmotic Regulation 126

5. Respiration 9. Cell and Tissue Metabolism

5.1 Anatomical Background 89 9.1 Enzymes in the Body of Cladocera 127
5.2 Environmental Background 89 9.2 Endocrine and Exocrine Secretion 128
5.3 Oxygen Consumption 90 9.3 Antioxidant System 129

v
vi CONTENTS

9.4 Effects of Toxic Compounds on Cytology and 14. Behavior

Metabolic Factors 131
9.5 Detoxification 135 14.1 Differences in Behavior Among Species 211
14.2 Migration and Swarming 212
10. Growth and Molting 14.3 Emotional Reactions 214
14.4 Impact of Xenobiotics on Behavior 216
10.1 Size and Weight Characteristics 137
10.2 Growth 137 15. Ecophysiology
10.3 Modification of Form 140
10.4 Molting 143 15.1 Physiological Background of the Limits of
10.5 Senescence 146 Environmental Factors 218
10.6 Impact of Xenobiotics 147 15.2 Adaptation 221
15.3 Genotypes 222
11. Reproduction 15.4 Environmental Conditioning by Cladocera 222
15.5 Cladocera in the Polluted Hydrosphere 224
11.1 Anatomical Background 151 15.6 Synergism and Antagonism Among Environmental
11.2 Cyclicity 151 Factors 226
11.3 Parthenogenetic Reproduction 152 15.7 Cladocera as Tools in Water Quality and Medical
11.4 Gamogenetic Reproduction; Diapause 155 Testing 227
11.5 The Physiology of Eggs and Embryos 157
11.6 The Physiology of Males 166 16. A Cytological Perspective
11.7 Sex Hormones 167 MARGARET J. BEATON, CARLI M. PETERS
11.8 Impact of Anthropogenic Factors on
Reproduction 171 16.1 Genome Size and Polyploidy 232
16.2 Cytogenetics 238
12. Locomotion 16.3 Endopolyploidy 241
16.4 Cytological Observations for Specific
12.1 Anatomical Background 175 Tissues 244
12.2 Environmental Background 177 16.5 Reproduction 249
12.3 Movement Trajectories 179 16.6 Concluding Remarks 252
12.4 Muscle Physiology 182
12.5 Immobilization 182
12.6 Fatigue and Stress 183 17. The Genomics of Cladoceran Physiology:
12.7 Impact of Toxicity on Locomotion 184 Daphnia as a Model
K. VAN DAMME, D. BECKER, E. TURNER,
13. Nervous System and Sense Organs J.R. SHAW, J.K. COLBOURNE, B. ZEIS,
M. CORDELLIER, E. DECAESTECKER,
13.1 Anatomical Background: Sense Organs 187 M.E. PFRENDER
13.2 Neurosecretion 189
13.3 Sense Organs 193 17.1 Introduction 253
13.4 Vision 194 17.2 History of Research: The Pregenomics Era 255
13.5 Effects of Electromagnetic Fields 205 17.3 Daphnia as a Model System for Physiological
13.6 Chemoreception 205 Genomics 257
13.7 Mechanoreception 206 17.4 Daphnia’s Ecoresponsive Genome 260
13.8 Endogenous Rhythms of Activity 209 17.5 The Genetic Basis of Physiological Plasticity: A Case
13.9 Effect of Xenobiotics 210 Study 263
 CONTENTS vii
17.6 Hunting for Physiologically Relevant Genes and 18.5 Nervous System and Sensory Organ
Regulatory Networks 268 Formation 290
17.7 Comparing Past to Present Physiologies 273 18.6 Gonad Formation 291
17.8 Future Directions: Exploring Physiological Variation 18.7 Hormonal Regulation of Embryonic
With Functional Genomics 275 Molts 292
Glossary Terms 278 18.8 Kairomones and Embryos 292
18.9 Osmoregulation in Embryos 294
18. Notes on the Physiology of 18.10 Respiration 295
Embryogenesis 18.11 Yolk and Glycogen 296
18.12 Miscellaneous Observations 296
A.A. KOTOV
Conclusions: Special Traits of Cladoceran
18.1 Short History 281
18.2 General Information and Staging 281 Physiology 299
18.3 Earlier Development: Cleavage, Blastulation,
Start of Segmentation, and Start of References 303
Neurogenesis 284 Index of Latin Names of Cladocera 387
18.4 Hox Genes and Expression of Other Genes 286 Subject Index 389
This page intentionally left blank
 List of Contributors

M.J. Beaton Mount Allison University, Sackville, M.E. Pfrender University of Notre Dame, Notre
NB, Canada Dame, IN, United States
D. Becker University of Virginia, Charlottesville, J.R. Shaw Indiana University, Bloomington, IN,
VA, United States United States
J.K. Colbourne University of Birmingham, Birming- N.N. Smirnov A. N. Severtsov Institute of Ecology
ham, United Kingdom and Evolution, Russian Academy of Sciences,
M. Cordellier Universit€at Hamburg, Hamburg, Moscow, Russia
Germany E. Turner Indiana University, Bloomington, IN,
E. Decaestecker KU Leuven Campus Kulak, United States
Kortrijk, Belgium K. Van Damme Senckenberg Research Institute and
A.A. Kotov A. N. Severtsov Institute of Ecology and Museum of Nature, Frankfurt am Main, Germany
Evolution, Russian Academy of Sciences, B. Zeis Muenster University, Muenster, Germany
Moscow, Russia
C.M. Peters University of British Columbia,
Vancouver, BC, Canada

ix
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 Preface

Increasing and universal environmental some issues are now clarified and some are
pollution stimulated numerous recent investiga- almost unknown.
tions in the pathological physiology of the Over 700 species of Cladocera (Crustacea:
Cladocera that brought forth abundant informa- Branchiopoda) are known and representatives
tion discussed in the present edition. In addition, of this group are often dominant in the fresh-
studies in normal physiology progressed in water fauna, sometimes occurring in enormous
various ways. quantities. They live in both small and large wa-
The structure of the previous edition is only ter bodies from arctic to tropical latitudes, in
slightly changed. However, new sections are open water, on the bottom, in mud, among
added and numerous new findings are intro- inshore vegetation, in acid pools on bogs, in
duced throughout the text. As well, misprints small accumulations of water in epiphytic
and errors are corrected. The present edition is plants, in narrow aquatic spaces between moist
supplemented mainly with data from sources sand grains. A few species even left the water
for recent years. and live in moist moss-like growth on tree trunks
Reviewing the results of the worldwide inves- in tropical cloud forests. Some species are
tigations one may note that they remain mostly specialized for life in saline lakes and in the sea.
confined to daphnids which live in open water, Cladocerans, especially Daphnia species,
especially to Daphnia, whereas representatives belong to the commonest animals in hydro-
of other families coping with different life condi- biology. They are counted, measured, weighed,
tions are still awaiting investigation. The vast cultured, their species lists are composed, distri-
and specific world of littoral and bottom-living bution in space and time described. Their role is
Cladocera is still waiting for due physiological recognized as the food resource of fish and as
assessment. Some data available for such species water quality indicators. Species of Cladocera
are discussed as well. Transformations of func- are described and redescribed nowadays in
tions and the related structures in different fam- excellent morphological detail.
ilies would be highly instructive and revealing. Usually, little more is taken into consideration
Probably, the present review will indicate what than a cladoceran as a living object with individ-
and how should further be studied in these ani- ual, mostly external, traits that permit species
mals which live very differently from pelagic recognition. There follows an attempt to summa-
species. Especially demonstrative would be, rize information showing that the Cladocera
e.g., data on transformations of the system of possess complicated and special metabolism
muscles and of the involved skeletal structures and behavior which deserve knowing, as these
performing different kinds of locomotion in rep- data may explain how and why Cladocera spe-
resentatives of various genera. cies successfully live in their various media.
Another special point of studies in Cladocera The following summary is an attempt to
physiology is that they are still fragmentary: contribute to a more profound understanding

xi
xii PREFACE

of how and why they participate in the processes of explanation is supplied by morphology (struc-
developing in inland waters. Particular chapters tural traits), e.g., thin skeletons, swimming ap-
of cladoceran physiology are still covered very pendages, oil drops, sometimes the presence of
unevenly. Recently, numerous and more in- slime, etc., in planktonic forms. However, phys-
depth data on pathological physiology are being iology makes a wide field which can be used for
accumulated, comparing with older data that understanding causative relationships.
were confined mostly to longevity and amount Daphnia is more and more frequently used in
of progeny as affected by xenobiotics. water-quality testing and as a model organism
Comparative physiological investigations of supposed to represent situations in natural or
representatives of various families with their artificial ecosystems (Lampert, 2011; Seda and
different ecology are urgently desirable and Petrusek, 2011).
would make a promising field. Of course, some- Along with special discussions, introductory
times more questions are raised than answers remarks are made whenever it seemed to be
supplied. The present review of this vast field necessary to make the matter useful both for spe-
is rather an attempt at systematic assembling cialists and for nonspecialists.
of the available data and demonstration of spec- The present review comprises studies made in
ificity of this group of crustaceans. Within the the period starting from the second half of
present context, the main attention is paid to the 19th century. Completeness of information
data demonstrating which and how the meta- was checked against Zoological Record, part
bolic links are influenced by particular natural 10 (Crustacea), vols 1e150 (for 2015) and
and anthropogenic factors in the hope of Russian Referativnyi Zhurnal (Biology, Zoology)
revealing the reasons of this impact. (1992e2015). Some earlier sources are also
Investigations of aquatic invertebrates added. Any incompleteness herein is because
frequently endeavor to obtain answers why a some fields are not yet investigated, some litera-
certain species is present or absent, why it is ture has not been found, and some points might
abundant, why it lives in a certain habitat. Part have escaped the author’s attention.
 Acknowledgments

The present volume is an attempt at making a sufficient for direct understanding of original
summary of work of many experts throughout texts. Many librarians, mostly personally un-
the world in various fields using special known to the author, retrieved numerous publi-
methods. A substantial contribution to physi- cations in different languages and times. Their
ology of the Cladocera has recently been made care and labor are appreciated, including those
by toxicologists. of Ms. N.I. Gotovskaya and Ms. E.V. Morozova
Special thanks are due to Dr. M.J. Burgis the Biological Department Library of the Russian
(United Kingdom) who generously used her Academy of Sciences (RAS). The facilities and
time and experience to make the manuscript of library of the Moscow Society of Naturalists
the first edition acceptable. were very useful, especially for earlier sources.
The present review is motivated by the Dr. V.R. Alekseev and Ms. N.M. Sukhikh were
author’s observations on living, mostly littoral, very helpful in work with resources of the li-
cladocerans. Both the initial training and subse- brary of the Zoological Institute RAS (St. Peters-
quent work of the author implied that hydrobiol- burg). I am sincerely grateful to Professor G.A.
ogy is impossible without physiological data. Boxshall (FRS; UK) for help in getting rare
Some recent observations are made at the publications.
Hydrobiological Station “Lake Glubokoe” My wife, L.A. Smirnova, Ph.D. (cited here as
(Russia). The author is grateful to his immediate L.A. Luferova) is tolerant (mostly) toward using
colleagues from the “Cladocera team” for help a big part of my time for such ventures as this.
and discussions: O.S. Boikova, N.M. Korovchin- Formulation of ideas included in this book
sky, A.A. Kotov, E.I. Bekker, and A.Y. Sinev. and its composition was much favored by
Dr. Kotov critically read the draft manuscript, creative environment at the Institute of Ecology
suggested numerous useful additions, and used and Evolution of the RAS, and by personal atten-
his skill for preparation of the manuscript and tion of academicians D.S. Pavlov and Yu.Yu.
figures. Dgebuadze.
The author is obliged to many teachers at The authors of Chapters 16e18 described
school and at the Linguistic University their special fields and made the subject much
(Moscow) for training in European languages more advanced and complete.

xiii
This page intentionally left blank
 Abbreviations and Units

Standard abbreviations and units are used.

ACh Acetylcholine
ATP Adenosine triphosphate
DHA Docosahexaenoic acid
DNA Deoxyribonucleic acid
DW Dry weight
EPA Eicosapentaenoic acid
FAs Fatty acids
GST Glutathione S-transferase
h Hour
Hb Hemoglobin
HUFAs Highly unsaturated fatty acids
IUs International units
MF Methyl farnesoate
mg% mg per 100 g
min Minute
MUFAs Monounsaturated fatty acids
NADH Nicotinamide adenine dinucleotide plus hydrogen
PCBs Polychlorinated biphenyls
PUFAs Polyunsaturated fatty acids
RNA Ribonucleic acid
RQ Respiratory Quotient
SAFAs Saturated fatty acids
TBT Tributyltin chloride
UVR Ultraviolet radiation
WW Wet weight

xv
This page intentionally left blank
 C H A P T E R

1
General
1.1 SYSTEMATIC POSITION worldwide fauna of Cladocera are available:
“Guides to the Identification of the Microinverte-
It is now thought that over 700 species of the brates of the Continental Waters of the World”
order Cladocera exist in the world fauna, many issues 1, Macrothricidae (Smirnov, 1992); 3,
of which develop enormous populations and Ctenopoda (Korovchinsky, 1992), 11, Chydori-
thus play a big role in the biosphere. New species nae (Smirnov, 1996); 17, Simocephalus (Orlova-
are still being described. Bienkowskaja, 2001), 13, The predatory
The Cladocera belong to the subclass Phyllo- Cladocera (Rivier, 1998); 21, Daphnia (Benzie,
poda of the class Crustacea. Most Cladocera 2005); 22, Ilyocryptidae (Kotov and Stifter,
belong to the orders Anomopoda and Ctenopoda. 2006), and 25, Eurycercus (Kotov and Bekker,
Anomopoda principally comprise the families 2016). There are also newer, general worldwide
Daphniidae (e.g., the genera Daphnia, Ceriodaphnia, resources for ctenopods, created by Korovchin-
Simocephalus, and Scapholeberis), Moinidae (Moina sky (2004); Leydigia (Chydoridae), by Kotov
and Moinodaphnia), Ilyocryptidae (Ilyocryptus), (2009); and Eurycercus, by Bekker et al. (2012);
Macrothricidae (e.g., Macrothrix and Streblocerus), as well as recent regional keys. As investigations
Acantholeberidae (Acantholeberis), Ophryoxidae, into Cladocera are actively developing, the
Eurycercidae (Eurycercus), Chydoridae (e.g., Chy- aforementioned summaries are rapidly
dorus and Pleuroxus), Bosminidae (Bosmina, Bosmi- becoming incomplete, and literature that is
nopsis). Ctenopoda comprise the families Sididae more recent should be considered.
(e.g., Sida, Pseudosida, and Diaphanosoma) and Hol-
opedidae (Holopedium).
Others belong to the order Onychopoda (the 1.2 GENERAL MORPHOLOGICAL
freshwater Polyphemus, as well as a few marine BACKGROUND
and brackish-water species) and the order Hap-
lopoda with the family Leptodoridae (Leptodora, As animal functions are linked to their form,
with two species). Both anomopods and cteno- some comments on the body structure and or-
pods produced species living on various sub- gans of Cladocera are provided here. Most of
strata and planktonic species. Onychopods and the animals attributed to the order Cladocera
haplopods comprise fewer species, all of which have the same principal structure, with various
are planktonic predators. modifications present in different species. Inves-
For reliable identification of the subjects in tigations into comparative and functional
physiological investigations, the keys to the morphology (such as, those by Fryer, 1968,

Physiology of the Cladocera

http://dx.doi.org/10.1016/B978-0-12-805194-8.00001-5 1 Copyright © 2017 Elsevier Inc. All rights reserved.
2 1. GENERAL

1974, 1991, etc.) have revealed exciting data on compressed from the sides, but many are
particular species, permitting a better under- spherical. In the case of Graptoleberis, there is a
standing of their lifestyles. curious and unique combination of lateral and
Cladocerans have inherited from their ances- dorsoventral compression. The appendages
tors a weakly segmented body covered with a have numerous, but organized, setae. The poste-
chitinous, mostly bivalved, shell and bearing rior end of the body (postabdomen) is bent at a
few pairs of appendagesdantennules, antennae right angle to the abdomen, or may even be
(biramous, with the single exception of female reversed. On the proximal dorsal side of the
Holopedium), mandibles, maxillulae, maxillae postabdomen, a pair of setae are present, tradi-
(may be completely reduced), mandibles, and tionally termed setae natatoriae (shown, e.g.,
five or six pairs of thoracic limbs in Figs. 1.3 and 13.1 right). All structures
(Figs. 1.1e1.4). Cladocerans are mostly oval, tend to undergo morphological radiation, and

C BP
HT
5c
EMB
TMM
SUS DVM
DLM
TMT
VLM
MG

DIV
A2MUS

FIB DAO

PA
END
CG
O AD RE
100 µm
A1 LM OCM ODM ENP LGC K L Mand DG LDS TLS

FIGURE 1.1 General anatomy of Acantholeberis curvirostris. A1, antennule; A2MUS, antennary muscles; AD, apodeme; BP,
brood pouch; C, carapace; CG, cerebral ganglion; DAO, dilator muscle of atrium oris; DG, duct of labral glands; DIV, divertic-
ulum; DLM, dorsal longitudinal muscles; DVM, dorsoeventral trunk muscles; E, compound eye; EMB, embryo; END, endo-
skeleton; ENP, endoskeletal plate; FIB, fibrils; HT, heart; K, keel of labrum; L, labrum; LDS, long distal setae of outer distal lobe
of limb 1; LM, levator muscle of labrum; Mand, mandible; MG, midgut; O, ocellus; OCM, esophageal constrictor muscles; ODM,
esophageal dilator muscles; PA, postabdominal lamella; RE, rectum; SUS, suspensory ligament; TLS, trunk limbs; TMM,
5c, transverse muscle of mandible; TMT, transverse mandibular tendon; VLM, ventral longitudinal trunk muscles. From
Fryer, G., 1974. Evolution and adaptive radiation in the Macrothricidae (Crustacea: Cladocera): a study in comparative functional
morphology and ecology. Philosophical Transactions of the Royal Society of London, B: Biological Sciences 269 (898), 137e274.
 1.2 GENERAL MORPHOLOGICAL BACKGROUND 3

E OL CG LM
Ca HS
O Oe
A2M
ODM
Mand
DES
LGC TMT
TMM
A2M
SUS
L
5c
Endo S
SA1
A2M

TL1

TL2 Ht

D Endo S
C
TTC
Mxlle

TL3 BP

MG

NC
FCS

FG
FP3
200 µm
A = ACAM
EX3 TL5 P = PCAM
EXS5 FP4
EXS3
EX4 TL4 AVS EP5

FIGURE 1.2 General anatomy of Daphnia longispina. A, anterior carapace adductor muscle; A2M, antennal muscles;
AVS, anterior vertical seta of trunk limb 5; Ca, caecum; D Endo S, dorsal endoskeletal sheet; DES, dorsal extension of ventral
endoskeletal sheet; EndoS, endoskeletal sheet; EP5, epipodite of trunk limb 5; EX3, 4, exopod of trunk limbs 3, 4; EXS5, exopod
seta 5; FCS, filter-cleaning spine of trunk limb 2; FG, food grove; FP3, gnathobasic filter plate of trunk limb 3; FP4, gnathobasic
filter plate of trunk limb 4; Ht, heart; HS, head shield; LGC, labral gland cells; Mxlle, maxillule; NC, nerve cord; Oe, esophagus;
OL, optic lobe of cerebral ganglion; P, posterior carapax adductor muscle; SA1, sensory seta of antennule; TL1, 2, 3, 4, 5, trunk
limbs 1, 2, 3, 4, 5; TTC, thickened trunk cuticle. Other abbreviations as in Fig. 1.1. From Fryer, G., 1991. Functional morphology and
adaptive radiation of the Daphniidae (Branchiopoda: Anomopoda). Philosophical Transactions of the Royal Society of London, B: Biological
Sciences 331 (1259), 1e99.
4 1. GENERAL

S1

S2
L
Ra
Rp
I
Vm2 Vm

a Sg3 b
Vm3

o.Lm
II
1

Sg4 c
III

o.Lm d Sg5 e
IV
V

f Asg1 Dm
Vm3

Ad

Vm2

Vm1

FIGURE 1.3 Muscles of Daphnia magna. From Binder, G., 1931. Das Muskelsystem von Daphnia. International Review of Hydro-
biology 26, 54e111.

homologous structures may occur in different the chitinous shell may be smooth, reticulated,
species in various forms, from the ancestral state ciliated, or variously honeycombed (see, e.g.,
to their complete disappearance or, in contrast, Kotov, 2013). The head shield of most species ex-
enlargement, and specialization. hibits head pores (Frey, 1959; Olesen, 1996), lead-
The body in most species is covered by the ing to an organ the function of which is probably
head shield and valves. The outer surface of ion exchange. Littoral cladocerans, which live
 1.2 GENERAL MORPHOLOGICAL BACKGROUND 5

FIGURE 1.4 Transverse section of Anchistropus emarginatus. 30 , promotor roller muscles; 40 , remotor roller muscles;
AM, adductor muscle of carapace; ASUS, accessory suspensory ligament; CCM, circular esophageal constrictor muscles; CE,
chitinous elaboration within carapace; HS, cuticle of head; MTM, major transverse muscles of mandibles; Mxille., maxillule;
S, sensory setae of antenna; ST, stomach; SUS, suspensory ligament; TL1, trunk limb 1; TMT, transverse mandibular tendon;
VCT, ventral carapace tooth. Other abbreviations as in Fig. 1.1. From Fryer, G., 1968. Evolution and adaptive radiation in the Chy-
doridae (Crustacea: Cladocera): a study in comparative functional morphology and ecology. Philosophical Transactions of the Royal Society
of London, B: Biological Sciences 254, 221e385, Fig. 115 on p. 341.

among organic and mineral particles and require The trunk segments are not numerous and the
protection, are supplied with thick chitinous outer structure is rather simplified.
shells, most with sculpturing; this increases the The inner organs are situated within the body
durability of their shells. In pelagic species, the rather loosely. The intestine may be straight or
integuments are thin. convoluted. Muscles do not form compact
The dorsal space under the shell is the brood masses and most of them can be seen individu-
chamber into which eggs are laid. ally (Figs. 1.1e1.4). The largest muscles are
6 1. GENERAL

longitudinal bands stretching along the gut. Darlington, 1957). In a general way, they are:
Groups of muscles allow motion of the thoracic Palearctic (including North Africa), Nearctic,
limbs and antennae. Small muscles rotate the Oriental (South Asia), Australian (see Smirnov
eye and move the labrum and antennules. and Timms, 1983; Van Damme et al., 2007a,b),
The intestine is supplied with circular muscles. Ethiopian (Africa south of Sahara), and Neotrop-
The ovary (or testis) is paired and situated ical regions. The Cape region is also clearly dis-
ventrally along the gut; this is also where the cerned (Smirnov, 2008). There are good reasons
fat body is situated (Fig. 4.13), in contact with (eight endemic Cladocera species) to discern
the ovaries (Jaeger, 1935). the Baikal region, as made by Starobogatov
There are two paired remains of the coelom: (1970) with reference to Mollusca.
the antennal gland and the maxillary gland (shell With reference to ctenopods, Korovchinsky
gland; Fig. 7.1). The latter is the organ of excre- (2004) suggests the Boreal region with the Palearctic
tion, whereas the antennal gland has no duct and Nearctic subregions, the Mediterraneane
and no outer orifice. Asian region with the MediterraneaneWest Asian
The nervous system comprises a double chain and East Asian subregions, the Paleotropical region
of ganglia, with the brain located in the cephalic comprising the South Asian and Australasian
region. Nerve fibers reach all structures, including subregions, the Central AmericaneSouth Amer-
remote ones. Sense organs comprise the unpaired ican region comprising the Neotropical and
eye, the unpaired ocellus (Figs. 1.1, 1.2, and 13.2), PatagoniceChilean subregions. Peripheral limits
sensory papillae situated on the antennule and on of geographic ranges of particular species are
some thoracic limbs (Fig. 13.8), and numerous mostly unknown.
tactile setae. The eye or the ocellus, or both, Some species are very widely distributed,
may be absent in some species. whereas others are restricted to very small
Each homologous structure in representa- geographic areas (e.g., some endemics of the
tives of various genera is a result of morpholog- Cape region). Navigation resulted in cases of
ical radiation, ranging from the ancestral transcontinental transfer of Cladocera, for
state to enlargement and specialization or to example, of Bythotrephes from Europe (Lake
reduction (sometimes complete disappearance) Ladoga) to North American Great Lakes (Bur
(Smirnov and Kotov, 2009, 2010). On the basis et al., 1986). Circumtropical species obviously
of the general structural scheme, three kinds of prefer high temperature, whereas some northern
specialization are formed: one used for collect- species do not expand their ranges to tropical
ing food from substrata (Fig. 1.1), another for latitudes.
filter feeding in open water (Fig. 1.2), and the Obvious differences exist in the interconti-
last, predatory. nental and latitudinal distribution of Cladocera
Further information on Cladocera may be species. Some species are clearly circumtropical
obtained from www.cladocera-collection.cz, and occur in latitudes where the limiting factor
Lampert (2011); Kotov (1913). is a high water temperature. High water temper-
ature is sometimes combined with slight salinity.
Some species are confined to northern latitudes
1.3 GEOGRAPHIC DISTRIBUTION or occur in the area of minimum winter temper-
atures. Differences in the geographic ranges,
Clear intercontinental differences exist in the obvious for many Cladocera species, may be
composition of the Cladocera fauna. More pre- confronted with the geochemical or hydrochem-
cisely, zoogeographic regions are discerned as ical provinces. It seems that little is done in this
formed due to geologic history (see, e.g., promising line.
 1.4 SPECIES-SPECIFIC EFFECT OF XENOBIOTICS 7
Studies of the Quaternary history of Clado- more tolerant to these metals, or their combina-
cera communities by skeletal remains in bottom tions, than other daphnids (Shaw et al., 2006).
deposits shed light on their state in the past and It was shown that Moina macrocopa was twice
trends of development (Frey, 1959, 1962; Ber- more sensitive than D. magna in 7-day toxicity
glund, 1986; Smol et al., 2001; Smirnov, 2010; test to perfluorooctane, sulfonic acid, and per-
Desellas et al., 2011). fluorooctanoic acid (Ji et al., 2008). The highest
sensitivity to the same concentrations of carbaryl
and methomyl (carbamate insecticides) was
1.4 SPECIES-SPECIFIC EFFECT OF manifested by Ceriodaphnia reticulata, the
XENOBIOTICS lowestdby M. macrocopa and Scaphleberis kingi
(Mano et al., 2010). D. magna is more severely
Different sensitivity to toxic substances was affected than D. pulex by diflubenzuron (Duchet
reported for different Cladocera species. Immo- et al., 2011). Sensitivity to insecticides imidaclo-
bilization by copper tested for 44 species was prid and fipronil was different (in descending or-
different: EC50 (effective concentration deter- der): in Ceriodaphnia, Moina, and Daphnia
mined in 48 h) was from 5.3 for Scapholeberis (Hayasak et al., 2012).
mucronata to 70.6 mg Cu/L for Disparalona ros- D. magna was less sensitive than Daphnia curvir-
trata (Bossuyt and Janssen, 2005). Comparative ostris to veterinary antibacterials (Bona et al., 2014).
tests of Cd and Zn on Daphnia magna, Daphnia Mechanisms of reaction to toxic blue-green
pulex, Daphnia ambigua, and Ceriodaphnia dubia algae were found to be different in D. magna
demonstrated that D. magna is significantly and D. pulex (Asselman et al., 2014).
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 C H A P T E R

2
Methods
Methods of investigating the physiology of anatomical background and function, as well
Cladocera range from direct observation of living as on the composition of food in the intestine.
specimens to recording the physical and chemical Intravital staining aids observation of func-
manifestations of particular physiological processes. tioning in living cladocerans. Various kinds of
intravital staining of the organ systems of Clado-
cera were originally elaborated by Fischel (1908).
2.1 METHODS OF COLLECTION The salivary gland can be stained using neutral
red and Bismarck brown (Cannon, 1922). In
Cladocera may be collected with planktonic thoracic limb IV of Eurycercus, there is a slime
nets and dip nets in the littoral and pelagic zones gland the secretions of which are stained bright
of large and small water bodies. They should be blue with Mallory’s stain (Fryer, 1962, 1963).
looked for in ponds, pools, puddles, temporary Gut contents have been stained with eosin,
pools, roadside ditches, acid bogs, fountains, all Congo red, methyl red, neutral red, and uranine
kinds of artificial basins, moist moss, and even for the determination of pH (Lavrentjeva and
in moist, moss-like growth on tree trunks. Usu- Beim, 1978). External slime may be distinguished
ally, a catch of a planktonic net contains many by placing a cladoceran in diluted Indian ink.
specimens belonging to several genera. Howev- Histochemical techniques have been used in
er, sometimes Cladocera may be absent or rare. the analysis of Holopedium slime (Brown, 1970).
The latter situation occurred, for example, in
water bodies of the Yucatan; though the faunal
list was rather long, large volumes of water 2.3 CULTIVATION
had to be screened to collect a few specimens
(Smirnov and Elias-Gutierrez, 2011). Quantita- Cultures started from a single female are
tive sampling (per unit volume or unit surface) called clonal cultures and provide relatively uni-
with special devices is used in limnology. form material. Culture methods, mostly for
Daphnia and Moina, have been described by
various authors either alone (e.g., Biotechnics
2.2 OBSERVATION OF LIVING of Daphnia Culture at Fish Farms, 1958; Dewey
SPECIMENS and Parker, 1964; Ivleva, 1969; Parker and
Dewey, 1969; Bogatova, 1973, 1980; Lampert,
Detailed examination of preserved or living 1975; Ten Berge, 1978; Goulden et al., 1982;
specimens supplies useful information on their Dodson et al., 1991) or in descriptions of particular

Physiology of the Cladocera

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10 2. METHODS

experiments. Cultured pelagic Cladocera should 2.4 IMMOBILIZATION AND

be fed with algae and adequate algal cultures ATTACHING
should be maintained for this purpose. Some
species (Daphnia magna and Daphina pulex) are Most cladocerans are very agile; therefore,
more easily cultivated than others. high-speed photography has been used (e.g.,
Gajewskaja (1940, 1948) suggested a method Storch, 1929; Zaret and Kerfoot, 1980) to study
of separating large-scale cultures of Cladocera them. Alternatively, methods to inhibit their
and algae because cultivation of Cladocera and movement have been devised. To retard quick
algae requires conflicting conditions. Since motion, Fryer (1968) immersed living cladoc-
then, methods of large-scale culture have been erans in an nontoxic viscid medium (“cellulose
developed further (Yalynskaya, 1961; Ivleva, nitrate”). Immobilization by narcotization is
1969; Lampert, 1975; Bogatova, 1992). The com- discussed in more detail in Section 12.5. Early
bined culture of Daphnia with other cladocerans techniques included attaching specimens to a
was suggested by Bogatova (1963). substrate on a glass slide using wax dissolved
A method was described for cultivation of in alcohol (Scourfield, 1900b; Pe~ nalva-Arana
Pleuroxus hamulatus individually in small vessels, et al., 2007). Porter and Orcutt (1980) used sili-
frequently supplied with fresh food (Galtsoff cone grease to fix D. magna by its head shield to
et al., 1937, p. 220). A similar method was used observe its feeding. For the purposes of his
for littoral Cladocera by Smirnov (1964, 1965a). study, Jacobs (1980) attached Daphnia by the
Fresh detritus was given at least every other caudal spine to a plasticine bed. Specimens
day (actually, a specimen was transferred to a thus immobilized could be observed and the
dish containing fresh detritus). Organic debris next instar was released into free water from
(detritus) was collected at shore bottoms and the attached exuvium.
screened to remove foreign animals. Using cyanoacrylate glue, Onbe (2002)
Artificial detritus prepared from plants was attached Pseudevadne and Evadne to the tip of a
also used in cultivation of Cladocera (see, e.g., glass capillary held in place by a stand to facili-
Rodina, 1963; Esipova, 1969, 1971; Dekker tate video recording. Pe~ nalva-Arana et al.
et al., 2006). Sterilization was used to demon- (2007) reported unbiased observations using
strate the role of bacteria in the alimentation of computer recording combined with the immobi-
Cladocera (Gajewskaja, 1938; Rodina, 1963; lization system.
Esipova, 1969, 1971). The latter author used a Methods of attachment were recently
diluted Lugol’s solution to minimize the described by Seidl et al. (2002) and used by
quantity of bacteria in food offered to Cladocera. Pirow et al. (2004) for investigating oxygen trans-
Suspensions of latex beads have also been port processes in D. magna. The latter authors
used in investigations of feeding behavior immobilized fasting animals by gluing their pos-
(Burns, 1968b, 1969; Hessen, 1985). terior apical spine with histoacryl to a bristle,
Preferences for environmental factors, and for which was then fixed to a coverslip with plasti-
food, may be ascertained by experiments on lin. Dye was then microinjected into the circula-
living specimens. Examination of food composi- tory system from the dorsal side into the space
tion is made easier by dissolving the soft tissues “directly downstream of the heart.” The cover-
of cladocerans with 3% sodium hypochlorite slip then formed the base of a thermostated
(Infante, 1978). This treatment may also be useful perfusion chamber in which an immobilized
for other purposes. daphnid was able to freely move its antennae.
 2.6 BIOCHEMICAL AND SPECIAL PHYSIOLOGICAL METHODS 11
Ivanova and Klekowski (1972) achieved
immobilization of Simocephalus by placing it
into the bulb of a Cartesian diver (used for deter-
mining oxygen consumption) and leaving no free
space around the animal, that is, it was too small
to allow movement. Photographic recording of
the heart rate and movement of thoracic limbs
has been used (e.g., Kolupaev, 1988). Further
on, computer recording of behavior is now
used (Pe~nalva-Arana et al., 2007).

2.5 MICROSCOPY
Various kinds of microscopy, including scan-
ning electron microscopy (SEM), can be used in
investigations of Cladocera (Kotov, 2013). A
variation of cladoceran preparation for SEM
was suggested by Laforsch and Tollrian (2000).
Modern video microscopy and digital image
processing methods take advantage of the trans-
parency of cladocerans (Colmorgen and Paul,
1995). Fluorescence analysis was originally FIGURE 2.1 The microscopic setup for partial pressure of
used by Pravda (1950). oxygen (pO2) imaging. A/D, analog/digital; PMT, photomul-
Surgical methods can be applied in investiga- tiplier tube. From Pirow, R., Wollinger, F., Paul, R.J., 1999a. The
importance of the feeding current for oxygen uptake in the water
tions of regeneration, vision, and neurosecretion. flea Daphnia magna. Journal of Experimental Biology 202 (5),
These are described by Ermakov (1927), Angel 553e562, Fig. 2.1 on p. 555.
(1967), and in Chapters 10 and 13.

Spectrophotometry has been used for the

2.6 BIOCHEMICAL AND SPECIAL identification of particular compounds, including
PHYSIOLOGICAL METHODS hemoglobin (Hb) (Karnaukhov et al., 1986).
Initially, Fox (1948) suggested that a quantitative
In biochemical and metabolic investigations, estimation of Hb content in Daphnia in arbitrary
special procedures, such as homogenization units could be obtained against a wedge-
(e.g., Guan and Wang, 2004b) and radiotracer shaped standard prepared from the worker’s
or chemical methods, have been used. There blood. Following this, cladoceran Hb was inves-
are various respirometric methods (Fig. 2.1. See tigated using spectral (Hildemann and Keighley,
also Chapter 5). Studies on homogenates using 1955; Hoshi et al., 1968) and chemical (Hoshi,
modern sensitive methods have opened up the 1963a, 1963b; Smirnov, 1970) methods.
possibility of investigating metabolic pathways. Recent toxicological studies have assessed the
Special techniques may be found in descriptions effects of xenobiotics on particular physiological
of the original investigations. processes.
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 C H A P T E R

3
Chemical Composition
3.1 LABILITY OF CHEMICAL The caloric content also changes in cladoc-
COMPOSITION erans exposed to xenobiotics. Thus, it somewhat
decreased in Daphnia schodleri exposed to hexa-
The chemical composition of the Cladocera is valent chromium (as potassium dichromate)
labile. In their body, relative quantities of physio- due to restructuring of its chemical composition
logically important constituents, those of no such (Arzate-C
ardenas and Martínez-Jer
onimo, 2012).
importance, or of xenobiotics vary depending on
the composition of the environment and of food.
Cladocera may accumulate useless or toxic sub- 3.3 PRINCIPAL CONSTITUENTS
stances. Furthermore, the chemical composition
fluctuates in the course of the molting cycle. There have been various determinations of
the chemical composition of some Cladocera
(daphnids, Moina, Bosmina, and Chydorus sphaer-
3.2 MOISTURE CONTENT AND icus). The general chemical composition of some
CALORIFIC VALUE Cladocera is shown in Table 3.2. The protein con-
tent ranges from 30% upward, the fat content is
The moisture content and calorific value of 1e20%, and the carbohydrate content is
some Cladocera spp. are shown in Table 3.1. 10e30%. Far more informative are reports on
Moisture content is usually within 80e90% and the dynamics of chemical composition, which
calorific value within 3e6 kcal/g dry weight depend on seasonal changes in a number of fac-
(DW). According to Sushchenya et al. (1990), tors, on starvation, or on other particular factors.
the dry matter content in Daphnia magna ranges Often, scattering of the data indicates depen-
from 7.4% to 10.6%, increasing at higher temper- dence on specific factors. Indeed, if arranged by
atures and higher food concentrations. season, chemical constituents demonstrate clear
The calorific value (kcal/g) is: Daphnia hyalina, composition changes, as shown, e.g., for Daphnia
6.3; Bosmina coregoni, 6.3; Chydorus sphaericus, pulicaria (in Fig. 3.2, from Heisig-Gunkel and
6.1; and Leptodora kindtii, 5.8 (Vijverberg and Gunkel, 1982). The chemical composition of
Frank, 1976). Variations in the calorific value Daphnia pulex generally confirms these data but
obviously depend mostly on the fat content. depends on the period of starvation, with rela-
Thus, the calorific value of “lean” D. magna is tive quantities of carbohydrate and fat
only 60% of that of Daphnia containing more fat decreasing, and those of protein and ash
(Chalikov, 1951). increasing (Fig. 3.1) (Lemcke and Lampert,

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itself, with its paraglossæ and labial palpi are sheltered beneath the
coping of the labrum and the lateral protection of the mandibles,
whilst the horny sheathing of the maxillæ protect the softer parts
folding underneath.
In the Apidæ, or normal bees, the basal joint has the same action
in withdrawing the entire organ into its place of rest; but the joint
which gives it this power is not in an analogous situation to that in
the Andrenidæ, for it is seated short of the joint which lies at the
base of the several organs of the cibarial apparatus. By bending
these downwards, it carries their apex backwards towards the basal
fulcrum through the action of these two joints, and, when there, the
more delicate ones are protected from abrasion or injury, by the
lateral overlapping of the horny skin of the maxillæ. All being thus
withdrawn within this covering, upon the joint which folds them
back, seated at the base of the tongue, the labrum falls, and further
to strengthen this protection, the mandibles close over it like
forceps.
That this difference in the arrangement of the cibarial apparatus
points to any distinctive peculiarities of economy has not been
ascertained, for the habits of the Scopulipedes greatly resemble
those of the Andrenidæ; although the habits of one of them,
Anthophora furcata, are remarkably like those of the foreign genus
Xylocopa, in its mode of drilling wood. But the Apidæ have cross
affinities amongst themselves, thus Ceratina resembles Heriades,
and some of the Osmiæ, in the way in which it nidificates.
The tongues of the Andrenidæ are always shorter, broader, and
flatter than those of the Apidæ, in which they are always long,
cylindrical, and tapering. In the first section of the Andrenidæ, the
paraglossæ are obtusely terminated at the apex, thence called
lacerated, and where they are fringed with brief bristles. The
peculiar form of the tongue in this section suggests its being
separated into two subsections, that organ being in the first
subsection very broad and bilobated, which gives those insects their
position in the series by approximating them to the preceding family
of the Diploptera, or wasps, whose tongues have the same bilobate
form, but each lobe in them is furnished with a gland. These
tongues, in both cases of the wasps and these bees, may conduce to
the building or plastering habits of the insects. The form may aid the
wasp and the Colletes, the first in the moulding of its hexagonal
papier-mâché cells, as it may the second in shaping and
embroidering the silk-lined abode of its embryonic progeny. Why
Prosopis should have this organization is difficult to conceive, unless
it be from an analogy of structure incidentally previously referred to,
beyond which any special object has hitherto escaped detection.
In the second section of the Andrenidæ, which have the
paraglossæ entire and terminating in a point, the tongues all also
terminate acutely with a lateral inclination inwards. In the
lanceolate-tongued tribe they bulge outwards laterally, although
pointed at the apex.
All this subfamily of Andrenidæ, excepting only the two genera
reputed parasites, viz. Prosopis and Sphecodes, are essentially
Scopulipedes, densely brush-legged, for the conveyance of pollen
which they vigorously collect; but from the brevity of their tongues
they are restricted to flowers with shallow petals and apparent
nectaria, their favourite plants being the abounding Compositæ and
Umbelliferæ, as well as the Rosaceæ, whence they derive the
agreeable odours which many of them emit upon being captured.
Their peculiar mode of collecting is a further reason for bringing
the brush-legged Apidæ collectively to the top of the normal bees, in
juxtaposition to the Andrenidæ, where the transition is made very
naturally from Dasypoda to Panurgus.
The whole of the cibarial apparatus, or trophi, is always complete
in all its constituent parts throughout the Andrenidæ; and it is only
with Ceratina, in the group of scopuliped Apidæ, that it begins to
show the tendency it has to abnormal deficiencies, by the
paraglossæ, in that genus, being obsolete. This characteristic, then,
exhibits itself in the Nudipedes with two submarginal cells who are
parasitical upon the Dasygasters, in whom also the maxillary palpi
participate in a deficiency in the authentic number of their joints,
whilst in Apis both maxillary palpi and paraglossæ are unapparent.
This shows that the numerical completion of the organs of the
mouth have nothing to do with the qualifications of the creature, the
best endowed in other respects being thus curtailed, the final cause
of which is not yet understood.
The shape of the tongue itself thus separates the Andrenidæ into
three well-defined divisions readily perceptible. These, as I have just
observed with respect to the differences in the mode of closing the
oral apparatus in both cases, yield no clue to economy and habits,
for which observation must supervene to illustrate it. This, patiently
carried out, is very desirable, as it is still in discussion whether,
notwithstanding the elucidation structure affords, Prosopis and
Sphecodes are or are not parasitical. Structure says they are, for, like
the cuckoo-bees forming the group Nudipedes in the Apidæ, they
are destitute of the requisite apparatus for collecting pollen. Mr.
Kirby, however, gives direct testimony in favour of Sphecodes being
a burrower, in the case of which bee it ought not to be a matter of
much difficulty to determine, for on sandy plateaus I have
occasionally found it very abundant, especially where there was
ragwort (Senecio) in flower in the vicinity, to which the males
resorted; but being at the time more intent on other matters, I
neglected the opportunity. Other observers concur with Mr. Kirby as
regards Sphecodes, and also say as much for Prosopis (better known
as Hylæus). I strongly incline to the opinion enunciated by Latreille
and Le Pelletier de St. Fargeau, that they are parasites. My opinion is
based upon peculiarities in them other than, although strengthened
by, the negative characteristic of absence of polliniferous organs. A
negative cannot be proved, it is true, yet what has been positively
asserted may as certainly result either from defective observation, or
from too strong a desire to find no parasites among the Andrenidæ.
My reasons occur elsewhere in this work, and I need not repeat
them. It is still an open question, and the young entomologist, if
entering the arena unprepossessed, might win his spurs in
determining it. It would be well worth the trouble of attending to for
those who have leisure, and if decided in favour of the independency
of these genera, which must be corroborated by a plurality of
observations, and not confined to one locality, they would form
strong and remarkable instances of a defective analogy in nature’s
workmanship, and suggest looking further for the causes of so
extraordinary an anomaly, and urge us to endeavour to trace the
equivalent which supersedes it.
The main subdivision of the Apidæ results from the habits of the
insects, which divides them into SOCIAL and SOLITARY. The only
tangible characters the social tribes present to distinguish them from
the solitary is the glabrous surface of the posterior tibiæ, with their
lateral edges fringed with bristles slightly curved inwards, and which
form, with the slightly indented surface of the limb, a sort of natural
basket for the conveyance of pollen or other stores to the nest. This,
however, has not been made use of as a main feature for scientific
distribution, although they might follow the Dasygasters, as
corbiculated bees, or little basket bearers, in which case they would
form as pertinent a group as any of the rest, and the whole
distribution of the bees, Apidæ, would then rest upon the absence
of, or the mode in which the polliniferous organs were present. But
the wonderful attribute of their extraordinary instinct prohibits their
being treated with the rest in a consecutive line, and renders it
rationally imperative that all the Cenobites should group together in
a section by themselves, and separate from the rest. Therefore in
my arrangement I have not availed myself of this very natural
character, and here indicate it, to show that I have not passed it
from not noticing it.
Although the division into social and solitary yields in itself no
tangible character whereby the insects may be separated, it being
wholly empirical, yet is it so natural and necessary that it is
impossible to gainsay it. We find the solitary section readily resolve
itself into groups or subsections, determined by positive structural
characters, indicative of certain habits, and having a conforming
economy, besides which they are equivalents.
 Thus the first subsection presents us with the brush-legged Apidæ
(Scopulipedes), which collect pollen upon their posterior legs. These
are further subdivided into those which collect it upon the whole
limb, viz. the coxa, the femur, the tibia, and first joint of the tarsus,
(the femoriferæ), and those which gather it merely upon the shank
and basal joint of the foot (the cruriferæ). These collectively form a
well-defined group, and why Panurgus should be separated from the
brush-legged bees, when it is a most conspicuous instance of the
faculty, even more so than any other of the Scopulipedes, I have yet
to learn. It is true its mode of collecting closely resembles that
practised by the Andrenidæ, as does also the furniture for the
purpose of its posterior legs, but being essentially collocated with
the Apidæ or normal bees by its tongue, it fittingly links itself to the
other brush-legged Apidæ (which have hitherto been placed
between the Dasygasters and the Social Bees), by means of the
genus Eucera, by reason of its two submarginal cells, the structure
of its maxillary palpi, its mode of burrowing, and by each being
infested by a similar parasite—a Nomada, which in accommodation
to the size of the sitos is the largest of the genus. Nomada does not
occur as a parasite upon any other of the brush-legged bees, or
indeed upon any other of the true bees at all, which peculiarity
brings these two genera into close contiguity to all non-parasitical
Andrenidæ, all of which have their legs furnished with polliniferous
brushes, and upon which subfamily, exclusively of these two
instances of Panurgus and Eucera, Nomada is solely parasitical.
With respect to the two submarginal cells to the wings, nature
must have some reason for the limitation, for we find it prevalent
also throughout the Dasygasters, or hairy-bellied bees.
The next very natural group is consistently central. It comprises
the cuckoo-bees, which are naked-legged (Nudipedes), by reason of
their parasitism, they not requiring organs to collect what they have
no occasion to use. Their parasitism extends both upwards and
downwards, those with three submarginal cells being parasitical
upon all the brush-legged bees, whether subnormal Andrenidæ or
the Scopulipedes, those with two submarginal cells being restricted
in their parasitism to the Dasygasters.
These Dasygasters, or hairy-bellied bees, form the next very
natural group. Their general peculiarity of structure I have had
occasion to advert to, in treating, in a former section of the work,
upon the structure of the imago, and to which I now refer to avoid
repetition. This group contains the majority of the artisan bees,
whose habits I shall particularize when I speak of the genera
specially; but we find carpenters amongst the Scopulipedes, and
essentially builders amongst the Cenobites, which form a further and
the last of our natural groups. A true cuckoo-bee (Apathus) consorts
amongst these Cenobites, and properly so, from many causes. The
anomaly would have been too great to have removed it to a place
amongst the Nudipedes, for although in obsolete paraglossæ, and in
a deficiency in the normal number of the joints of the maxillary
palpi, it resembles some of these, its general habit and general
structure, bating that controlled by its parasitical habits, are so like
Bombus, that it cannot well be separated far from the latter,—
especially as we know too little of its habits to say that it does not
regularly dwell in the nest of its sitos, which may well mistake it for
one of its own community, it resembling the species it infests so
closely; it therefore consistently associates systematically with the
temporarily social societies.
Having thus cursorily skimmed the surface of the method I
suggest, I have next to give my reasons for proposing it in lieu of
adopting any yet extant.
My exhibition of Kirby’s grouping, in the preceding section, where
I treat of the scientific cultivation of British bees, will fully explain
why I could not adopt that arrangement.
Why I cannot follow Latreille’s, is, that in his last elaboration, in
his ‘Families Naturelles,’ published in 1825, which must be
considered as his final view, he does not satisfactorily divide the
Andrenidæ, of the genera of which he has made a complete jumble.
With the Apidæ in his group of Dasygasters, he intermixes Ceratina,
separating it from the group of Scopulipedes, where it truly belongs
by every characteristic, and he mingles also with them the two
cuckoo genera Stelis and Cœlioxys, which are merely parasites upon
these Dasygasters, and can only be associated by the structural
conformity of the two submarginal cells to the superior wings, and
the length of the labrum, the latter being a character of very
secondary importance; and further, he dissevers the Scopulipedes in
placing Panurgus at the commencement of the Apidæ, and the rest
proximate to the social bees.
Westwood, in his modification of Latreille’s system, certainly
divides the Andrenidæ better than his master had done, but he does
not go far enough. Besides, he interposes Halictus and
Lasioglossum, (the latter admitted as a genus merely out of courtesy
to Curtis, who had elevated it to that rank in his ‘British Entomology,’
although it is nothing more than a male Halictus), between
Sphecodes and Andrena with Cilissa, these having lanceolate
tongues with lacerate paraglossæ, whereas Halictus has a very acute
tongue, and its paraglossæ are entire, as is also the case with
Dasypoda, from which Halictus is thus divided. In the Apidæ, he
does not separate the cuckoo-bees, but with Latreille intermixes
Cœlioxys and Stelis with the artisan bees, although without retaining
Latreille’s convenient and suitable name of Dasygasters, for this
group of mechanics. The same objection I take to his Scopulipedes
as that expressed above, relative to Latreille’s.
Precisely the same fault I find with the Andrenidæ of Smith, as
that urged above with respect to Westwood’s. He is more careful
with his Apidæ, his Cuculinæ being all genuine parasites, but he
includes Ceratina with the Dasygasters, with which it has no affinity
of structure, and only a slight analogy in the form merely of its
abdomen without its hairiness beneath, to that of Osmia, from
whose proximity he takes it to place it near Heriades, when it is
certainly intimately allied in every respect with the Scopulipedes, and
by reason of its subclavate antennæ might suitably be brought into
juxtaposition with Panurgus, did not its obsolete paraglossæ and
three submarginal cells interfere with its occupying this position. To
his Scopulipedes the same objection is valid as that taken to
Latreille’s and Westwood’s disposition of them. Amongst the social
bees he separates Bombus from Apis, by the intervention of
Apathus, which is scarcely consistent.
It is in no spirit of captiousness that these objections are made;
they are deduced from collocations whose conspicuous incoherence
is patent to the most superficial observation. The distribution I have
here introduced has been made merely to ameliorate, and make
more cogent, what was so palpably defective and feeble.
 CHAPTER IX.

A TABLE, EXHIBITING A METHOD OF DETERMINING THE GENERA OF BRITISH

BEES WITH FACILITY.

The following table is constructed exclusively to facilitate, by the

most obvious characters, the recognition of the several genera into
which the family is divided; it will, however, be incumbent upon the
learner to use some diligence in order to acquire an accurate
perception of their distinguishing characteristics.
By the present extremely artificial plan the systematic sequence is
disturbed; but the numbers, which will be found appended to the
names in the table, will show their orderly succession.
The natural generic character which precedes the account of each
genus in the next division of the work will give the reason, by
comparison, of the order in which “system” arranges them, and
which being based mainly upon the differences of the trophi,—
although, conjunctively with other characters, the trophi must
necessarily be studied for its explanation,—their description in the
description of the part of the imago is consequently referred to.
Did we know exactly the uses of the component parts of the
trophi severally, we should be better able to determine the
legitimacy of applying them to the purpose of indicating the natural
generic character, but being compelled, by reason of our ignorance
of their several special functions, to avail ourselves of their form,
relative proportions, and number only, uncertainty of having caught
the clue of nature’s scheme must of necessity attend this
distribution.
But as what we do know of their uses in this family clearly
indicates them to be an essential instrument indispensable to the
economy of the insect, and which gives these organs an almost
paramount importance, their comparative construction in the several
genera would yield clear notions of the true order of succession,
were we acquainted with the relative significancy of the various
portions of the entire organ. Thus we see it numerically most
complete in what we are pleased to suppose the least genuine bees
—the Andrenidæ.
In my series of the genera proposed in the preceding section, with
the Nudiped true bee Melecta commences a deficiency of either
some of the joints of the maxillary palpi, or of the paraglossæ;—
throughout the artisan bees this abridgment is conspicuous both in
number and proportion; and it culminates in what we consider the
facile princeps, that most wonderfully organized of all insects—the
genus Apis, which in its neuters has neither paraglossæ nor
maxillary palpi, the latter being equally deficient in the male or
drone, and in the queen; and in both the male and the queen the
paraglossæ are but rudimentary.
Nature appears too mysterious in her operations to permit us to
solve these remarkable anomalies, for no combination of the genera
founded exclusively upon them supplies us with Ariadne’s thread.
Every such combination breaks up more harmonious groups, and we
then retrace our steps, satisfied that we are on the wrong road.
In some other orders of insects the cibarial apparatus has but little
bearing upon the insect’s mode of life, for in many it is not used
either for nutrition or in their economy, or so slightly so as to admit
of its being considered of very inferior importance, although
systematists—to enhance the value of their own labours, by the
frequent difficulty, from excessive minuteness, of its examination—
have usually made it a prominent feature in their arrangements.
 That science has not widely strayed away from the true succession
and natural affinities by the main selection of the trophi for the
arrangement of the bees, seems partially confirmed by the
gradations of form or habit that this method of treatment in general
exhibits. A higher method doubtless exists, which would give form,
number, and proportion very inferior rank in ordering the
arrangement, but at present the clue to it has not been discovered.
These questions are indeed beyond the scope of a work of this
character, which is merely a ladder to the fruits of learning, and the
bearing of them is only hinted at to indicate that there is much
exercise for the intelligence in the study of even this small family.
The mind that would stop in the study of nature at the knowledge of
genera and species, can be very speedily satisfied, and one bright
spring day’s successful collecting will furnish the materials for much
patient and industrious occupation.
In nature we find all things apparently blended in the grandest
confusion; but they all have mutual and reciprocal bearings which
give a definite purpose to the seeming disorder, and which make
each separate unit the centre of all. But we, from our inability to
grasp in its fulness the order of this disorder, are obliged to seize
fragments and, separating them into what we conceive to be their
coherent elements, use them as exponents of the entirety. They
could not so exist in nature, but would speedily die out, and it is only
by the way in which we find them intermingled, that they can be
maintained. Thus, as all conduce to the conservation of each, each
conduces to the conservation of all.
A large collection of natural history, composed of every available
item that can be gathered from every kingdom of nature’s vast
domain, may perhaps be compared (magnis componere parva) with
the constituent parts of a most elaborately-constructed and
complicated clock, which its skilful artificer has designed and made
to record and chime the divisions of time, and to register the days,
weeks, months, and seasons, and which a virtuoso having taken to
pieces, has sorted into its details of wheels and springs, levers and
balances, chains, bells, and hands, which told the time when its
music would peal; and arranging like to like, thinks he will thus
understand more clearly the complexity of the varied movements.
But, sadly disappointed, he finds he cannot comprehend the
combination of the intricate machinery, although he singly admires
the minute perfection of each delicate and ingenious piece lying
before him which composed the structure, but which has now lost all
expression, his curiosity having deprived the organism of its vitality,
which is its most wonderful element.
And this is our process, for if we stop here we have but an
assortment of vapid machinery, no click of whose wheels gives note
of the vital hilarity of their relative and combined effects. The final
cause of creation escapes us thus frittering it into details, which if
we merely abide by, we but loiter at the foot of Pisgah, instead of
ascending its summits to survey thence the sunny and varied
landscape, the glorious sea, and, arching over all, the blue cope of
heaven. The manifold relations of animate and inanimate nature,
which, although they must be studied in detail, are to be appreciated
in their entirety, should stimulate the efforts of the naturalist to
conquer all impending difficulties, and he should not permit himself
to be satisfied with this preliminary knowledge.
Although the above be the inevitable effect of distributing nature
into its component parts, it is the indispensable precursor to the
study, for the scientific treatment is the only mode whereby, through
special study, we can arrive at the comprehension of the great
generality. We thus strive to trace the mode in which each emanates
from each; and even when this is not absolutely tangible we may
discover affinities or analogies by structural resemblances which
implicitly lead to physiological inferences, and thence on, higher and
higher, all lending us aid to make the larger survey, wherein we
behold the concatenation of the many links which harmonize the
spiritual with the material. But the study must be thorough, and its
details are not to be spread out before us merely as a beautiful
picture-book. They all have their place in the great ordinance of
nature, which it is for us to find. At first we can only spell the
syllables, which the study of species puts together for us, but by
degrees we shall trace the words, and read the sentences: a study
more abstruse but far more pregnant than that of the Egyptian
hieroglyphics, and whose attainment is rewarded with a supremer
knowledge than is accorded by these, which exhibit merely the
legends of dead despots; but here we have a display of the vitality
of the wisdom inscribed in gleaming characters upon the leaves of
the wonderful book of life, God’s glorious works, made manifest to
man.
Thus we should aim at the knowledge of final causes, the
apparent wisdom of whose adaptations points clearly to the source
of all—the first great Cause. A naturalist with such large views has a
wide field before him, which with every step expands, and which
alone is worthy of engrossing the earnest attention of his
intelligence, and is in itself sufficient to absorb the profoundest
contemplation. His mind becomes thus filled with great objects,
which charm it with their beauty and feed it with the complexity of
their intricate combinations, whose earnest development is an
affluent stream of perpetual instructive occupation. With Newton we
may say: “We everywhere behold simplicity in the means, but an
inexhaustible variety in the effects,” resulting all from the luminous
wisdom of prearranged design.
The humiliation which attends the sentiment of the utter inability
and incompetency of the mind to grasp the intricacy and vastness of
nature, is consoled by the redundant proofs the contemplation yields
of a supreme and benevolent Providence presiding over all things,
and thence we derive the comfortable and supporting assurance, in
the fickle waywardness and vicissitudes of a harassed and anxious
life, that a benevolent eye is ever watchfully awake; for the
naturalist everywhere beholds that omnipotently wise and loving
Providence in active operation throughout nature.
No study like natural history, pursued in a humble and docile spirit,
so harmoniously elicits the religion of the soul, or than which so fitly
prepares it to enter, by the pathway of the works of God, the august
temple of His revealed Word.
But to return: what we call science is the mere accidence of
nature, which in fact aggravates our infirmity by permitting our
intelligence to attempt to grasp, through the various details, their
intricate combinations. But as truth sooner arises out of error if
methodically pursued, and its results recorded, than out of confusion
and guesswork, theories based upon observation, however
inaccurate at first, ultimately lead up to the certain acquisition of the
truth itself.

AN EASY DISTRIBUTION OF THE BEES,

THE NUMBERS REFERRING TO THE SCIENTIFIC SERIES.

Andrenidæ (Subnormal Bees).

TONGUE SHORTER THAN THE MAXILLÆ, PORRECT.

Posterior tibiæ clothed with hair to convey pollen.

 Two submarginal cells.
Posterior legs very robust, polliniferous
hair on tibiæ and plantæ
dense but short - Macropis (7).
Posterior legs slender; polliniferous
hair on femora, tibiæ, and plantæ
dense and very long - Dasypoda (8).

Three submarginal cells to the wings.

Abdomen truncated at base - Colletes (1).
Abdomen ovate.
Abdomen entire at apex; maxillary
palpi as long or longer than
the maxillæ - Andrena (4).

Abdomen entire at apex; maxillary

palpi half the length of the
maxillæ - Cilissa (5).
Abdomen with a vertical incision
at the apex - Halictus (7).

Posterior tibiæ without hair to convey pollen.

Two submarginal cells to the wings. - Prosopis (2).
Three submarginal cells to the wings. - Sphecodes (3).

Apidæ (Normal Bees).

Tongue as long or longer than the maxillæ, inflected beneath, and
covered by the maxillæ in repose.

Without polliniferous organs.

Two submarginal cells to the wings.
Abdomen at apex rounded - Stelis (17).
Abdomen at apex conical - Cœlioxys (18).
Three submarginal cells to the wings.
Abdomen lanceolate - Nomada (14),
Abdomen subtruncate at base.
Abdomen obovate, thorax glabrous - Epeolus (16).
Abdomen subconical, thorax hirsute - Melecta (15).
Entire body densely hairy - Apathus (25).

With polliniferous organs.

Pollen conveyed on the venter.
Two submarginal cells to the wings of all.
Abdomen subclavate.
First three joints of labial palpi
continuous, terminal joint inserted
before apex of third - Chelostoma (21).
First two joints of labial palpi
continuous, two last inserted
before the apex of the second - Heriades (22).
Abdomen obovate, rounded at apex - Osmia (24).
Abdomen truncated at base.
Segments slightly constricted,
and not spotted with colour - Megachile (19).
Segments not constricted,
spotted with yellow - Anthidium (20).
Pollen conveyed on the posterior legs.
Two submarginal cells to the wings.
Abdomen lanceolate; antennæ
clavate; posterior legs covered
with long hair - Panurgus (9).
Abdomen obovate; antennæ filiform;
posterior legs covered
densely with short hair - Eucera (10).
Three submarginal cells to the wings.
Short dense hair on the whole posterior
tibiæ externally.
Abdomen obovate; first joint of
labial palpi twice as long as
second - Anthophora (11).
Abdomen subrotund; first joint
of labial palpi six times as
long as the rest - Saropoda (12).
Long hair, but loose, on the entire
posterior tibiæ, externally
and internally.
Abdomen subclavate - Ceratina (13)
 Curved hair fringing the edge only
of the posterior tibiæ, the
centre glabrous.
Body densely hirsute, spurs to
all the tibiæ - Bombus (26).
Body subpubescent, no spurs
to the posterior tibiæ - Apis (27).

It will be desirable to add a few observations to the preceding

table to facilitate its use, and because, as many of the characters
upon which it is framed are exclusively those of the female, it is
necessary to point out the differences of their males, that the sexes
of the genera may be duly recognized and associated.
It may be first noticed generally that the antennæ, in the males,
are not usually geniculated at the scape, which is nearly always the
case in the opposite sex, and they are also, with rare exceptions,
always longer than those of their females. In Colletes, Prosopis,
Dasypoda, Panurgus, Ceratina, Nomada, Melecta, Epeolus, Stelis,
and Anthidium, the habit or colouring of the males is so similar to
that of the females, that their genus may be thus at once
determined, and, in fact, the brief characters in the table will
embrace them.
The male Eucera can be distinguished from those of Anthophora
and Saropoda, both by the differences in the number of the
submarginal cells of the wing, and by the extreme length of its
antennæ, whence the genus derives its name. In Andrena and
Cilissa, the males have usually lanceolate bodies. In the latter genus
there will be no difficulty in associating the legitimate partners; but
in Andrena, although general habit will usually bring the male within
the boundary of the genus, nothing but experience, or specific
description will associate the sexes correctly, there being in many
cases an extraordinary discrepancy between them. These two
genera themselves also can scarcely be distinguished apart,
excepting by means of their trophi; Cilissa, however, in general habit
greatly resembles the genus Colletes, especially the Cilissa tricincta,
which might, upon a superficial glance, be almost mistaken for one
of them.
The male Halicti have long cylindrical bodies and long antennæ,
but from the male Chelostoma, which has a very similarly shaped
body also and long antennæ, they may be distinguished by the
differences in the number of the submarginal cells; and from those
of Sphecodes, by the antennæ, which, in the latter are not relatively
so long, and are usually moniliform. The thorax of these is also less
pubescent, and the tinge of the red colour of their abdomen is
different from that of the red male Halicti.
The males of Cœlioxys can be readily distinguished from those of
Megachile, by the spinose apex of their abdomen. In Megachile,
general habit will bring the males within the precincts of their genus,
as well as their largely dilated anterior tarsi in some of the species.
A difficulty similar to what is found in the distinction between
Andrena and Cilissa, arises in the separation of Chelostoma from
Heriades, and which we shall again meet with in drawing the line
between Anthophora and Saropoda. The difference can only be
detected by examining the trophi, but a pin and a little patience will
elucidate the separation. The males in all but two species of
Anthophora may be readily associated with their partners; but in
these two the females are entirely black, and so hirsute as to have
led Ray (wanting the knowledge of the use of the trophi and
posterior shanks) to unite the one he knew with his Bombylii; their
males are fulvous, and the latter have a remarkable elongation of
the intermediate tarsi, from one of the joints of which also a tuft of
hair or a loose lateral fringe projects, giving them thus a wider
expansion, and the use of which is prehensile, the same as that for
which the anterior tarsi in some of the Megachiles and in our single
Anthidium receive their dilatation. This structure has also the effect
of adding very considerably to the elegance of their appearance
when they are in fine condition.
 The male Apathi can only be distinguished from the male Bombi
by familiarity with specific characteristics, or by the examination of
the trophi. But the former is the more certain mode of separation, as
the trophi in Bombus vary in some species, but not sufficiently to
authorize generic subdivison. General appearance will mark where
they approximately belong. The length of their antennæ sufficiently
distinguishes them as males, and they may be taken with impunity
in the fingers from flowers for examination, being, like all the male
aculeate Hymenoptera, unarmed with stings. The female Apathi may
be superficially distinguished from the female Bombi, which they
most resemble, exclusively of the generic characters of the convex
and subpubescent external surface of the posterior tibiæ and the
trophi, also by their abdomen being considerably less hirsute than
that of the genuine Bombi, in which it is entirely covered with dense
shaggy hair, whereas in Apathus there is a broad disk upon its
surface nearly glabrous. If I remember rightly, it is the male Apathi
only, and not the male Bombi, which emit on capture a pleasantly
fragrant odour of attar of roses.
The table will suffice for distinguishing the male Apis from all other
male Apidæ, and which has a further peculiarity exhibited by no
other of our native bees, in the conjunction upon the vertex of the
compound eyes, in front of which, upon the frons, the simple eyes or
ocelli are placed in a very slightly-curved line.
These indications are enough to enable the beginner to work his
way smoothly, and a little practice will soon render these
observations superfluous.
The economy of nature is so perfect that wherever we can trace a
difference, we may assume that a reason and a purpose exist for the
variation. Thus we do not know why some bees have three
submarginal cells to their wings, and others only two. Nor do we
know what governs their variety of shape. The deficiency we might
think implied inferiority; but this cannot be, for those with most
frequently the smaller number, viz. the artisan bees, are, in the
majority of cases, the most highly endowed, and have the most
special habits.
In the relative numbers of the maxillary and labial palpi, there are
remarkable differences, the reason for which we cannot trace, for, as
before observed, we do not know even their function, which would
perhaps guide us to other views. Their normal numbers are six
maxillary, and four labial palpi. The latter take remarkable relative
development and peculiarity of insertion and form, especially in the
Apidæ; but throughout the whole series of our bees, they are never
reduced to fewer than their normal number, whereas the maxillary
palpi never have similarly large development of structure, and are
variously modified in number and consistency from the typical or
normal condition.
Thus in Eucera and Melecta there are but five joints; in Osmia and
Saropoda, four; in Chelostoma and Cœlioxys, three; in Anthidium
and Megachile, etc., two; and in Epeolus and Apis but one.
In this collocation no incidental peculiarity beyond diversity is
apparent, for in the first instance a parasite and a bee not parasitical
are associated; and in the last, a parasite is associated with the bee
which has the most elaborate economy, and the most largely
developed instinct of all known insects. Nor are, in any case, those
parasites associated by these means with their own sitos, or insect
upon which they are parasitical.
Thus encouragement attends the beginner at the very outset of
his study; and the prospect of a wide field for discoveries, in many
directions, lies open to him, to excite his curiosity and to stimulate
his industry to the pursuit of higher aims than the mere
accumulation of species.
 CHAPTER X.

THE SCIENTIFIC ARRANGEMENT AND DESCRIPTION OF THE GENERA, WITH

LISTS OF OUR NATIVE SPECIES AND AN ACCOUNT OF THE HABITS AND
ECONOMY OF THE INSECTS, WITH INCIDENTAL OBSERVATIONS SUGGESTED BY
THE SUBJECT.

I now proceed to the treatment and description of the genera

severally, and the enumeration of the species in due scientific
consecutive order.
The generic names adopted are those of the first describers of the
genera; but the generic characters given by them could not be
employed, they having been usually framed to suit special purposes.
All the generic characters introduced into this work are therefore
quite original, and have been made from a very careful autoptical
examination of the insects themselves.
The synonymy added to the lists of species is limited to the
species described in Mr. Kirby’s work, where he is not the first
describer, or to those of such other English works wherein the
species may have been described in ignorance of its previous
registration.
The observations appended, wherein the habits of the insects are
described, will be found to embrace discursive subjects suggested by
the matter in hand, and here a dry didactic style has been purposely
avoided, as in the majority of cases they record the personal
experiences or notions of and hints from an old practical
entomologist.

Class INSECTA METABOLIA, Leach.

Order HYMENOPTERA, Linnæus.

Division ACULEATA, Leach.

Antennæ in male with 13 joints, in female with 12. Abdomen in male with 7
segments, in female with 6.

Family MELLICOLLIGERÆ (Honey collectors), Shuck.

Subfamily 1. Andrenides (Subnormal Bees), Leach.

Syn. Genus Melitta, Kirby.

The maxillary palpi always six-jointed.

Section 1. With lacerate paraglossæ.

Subsection a. Linguæ emarginatæ (with emarginate tongues).

Syn. Obtusilingues, Westw.

Three submarginal cells to the wings.

Genus 1. Colletes, Latreille.

(Plate I. fig. 1. ♂ ♀.)

Melitta * a, Kirby.

Gen. Char.: Head transverse, flattish; ocelli in an open triangle on

the vertex; antennæ not geniculated, but slightly curved, filiform,
short; joints, excepting the basal or scape, which is as long as five of
the rest and slightly curved, nearly equal; face beneath and within
the insertion of the antennæ, slightly protuberant, laterally flat or
concave; clypeus convex, margined anteriorly, entire; labrum
transverse, slightly produced in the centre in front, and the process
rounded; mandibles obtuse, subbidentate; cibarial apparatus short;
tongue deeply emarginate and bilobate, the lobes fringed with short
setæ; paraglossæ half the length of the tongue, abruptly terminating
and lacerate, and setose at the apex; labial palpi much shorter than
the paraglossæ, four-jointed, the joints equal and each subclavate;
labium about the same length as the tongue, its inosculation acutely
angulated; maxillæ broad, lanceolate, the length of the tongue;
maxillary palpi six-jointed, not so long as the maxillæ, the two basal
joints the longest, the rest equal, short, and subclavate, the apical
one rounded. Thorax subquadrate, very pubescent, the prothorax
inconspicuous; scutellum transversely triangular or semilunate,
postscutellum lunulate; metathorax abruptly truncated, and densely
pubescent, especially laterally, for the conveyance of pollen; wings
with three submarginal cells and a fourth slightly commenced, the
second and third each receiving about their centre a recurrent
nervure; legs all pubescent, the anterior and intermediate on their
external surface chiefly, their plantæ also setose; the posterior
coxæ, trochanters, femora, and tibiæ very hirsute, especially
beneath, their tarsi entirely setose; claws bifid. Abdomen truncated at
the base, subconical with a downward bias, the segments with
bands of closely decumbent nap, and the surface of all more or less
deeply or delicately punctured; the basal segment in the centre,
beneath, with a longitudinal tuft of long hair.
The MALE differs in having the mandibles more distinctly bidentate,
and in being less densely pubescent, especially upon the legs. In
general aspect it is very like its female.
Note. The genus Cilissa has, superficially observed, much of the
habit of Colletes, particularly in the male of Cilissa tricincta.

NATIVE SPECIES.
 1. succincta, Linnæus, ♂ ♀. 3½-5½ lines.
succincta, Kirby.
fodiens, Curtis.
2. fodiens, Kirby, ♂ ♀. 3½-4½ lines.
pallicincta, Kirby, ♀.
3. marginata, Linn., ♂ ♀. 3-4 lines.
4. Daviesiana, Kirby, ♂ ♀. 3½-4½ lines.
(Plate I. fig. 1 ♂ ♀.)

GENERAL OBSERVATIONS.
This genus is named from κολλήτης, one that plasters, in allusion
to the habits of the insects, which will be described below. The
female insects themselves have, at the first glance, very much the
appearance of the working honey-bee, but they are considerably
smaller, and, upon a very slight inspection, they are found to be
exceedingly distinct. The respective males of the species are
conspicuously smaller than their females, but their specific
characteristics are very much alike, and there is some difficulty in
separating and determining the species. One strong peculiarity,
marking all of them, is that the segments of the abdomen are
banded with decumbent, hoary or whitish down, in both sexes, and
the determination of the species lies chiefly in the variations of these
bands, and in the almost entire absence or conspicuous presence of
minute punctures covering the segments. The females are very
active collectors of pollen, and return from their excursions to obtain
it, very heavily laden to their nests. I am not sure that all the species
are not gregarious, to use this term in an acceptation somewhat
different from its usual application, for here, and whenever used in
entomology, it is meant to signify that they burrow collectively in
large communities, forming what is called their metropolis, although
each bores its independent and separate tube, wherein to deposit its
store of eggs. The males, neither in these insects nor throughout the
whole family of the bees, participate at all in the labours required for
the preservation and nurture of the progeny, a duty that wholly
devolves upon the maternal solicitude of the female,—these males
having fulfilled their mission, which is not perhaps restricted to their
sexual instinct, but may also be conducive to the grand operation of
the family in the economy of nature, viz. the fertilization of the
flowering plants, flit from blossom to blossom, and thus convey
about the impregnating dust. They may also be often seen basking
in the sunshine upon the leaves of shrubs, and thence they become
lost or dispersed or the prey of their many enemies,—birds or
insects, which are always on the alert in search of ravin.
The aspect selected by the females for their burrows, varies
according to the species. Some choose a northern, and others a
southern aspect; thus, the C. succincta seems to prefer the former,
and the C. fodiens the latter, as does also the C. Daviesana; and
where they burrow they congregate in enormous multitudes. The
mortar interstices of an old wall, or a vertical sand-rock, which, from
exposure, is sufficiently softened for their purpose, are equally
agreeable to them; nor have they any objection to clay banks.
In these localities each individual perforates a cylindrical cavity,
slightly larger than itself, and which it excavates to a depth of from
eight to ten inches, or even sometimes less. Now comes into
operation the use of the peculiarly-formed tongue with which nature
has furnished them, and described above in the generic character.
These cells are occupied by a succession of six, or eight, or even
sometimes no more than two, three, or four cartridge- or thimble-
like cases, in each of which is deposited a single egg with a
sufficiency, taught the creature by its instinct, of a mingled paste of
honey and pollen, for the full nurture and development of the
vermicle that will proceed from the egg upon its being hatched, and
wherein this larva, having consumed its provender, becomes
transformed into the pupa, and by the continuance of nature’s
mysterious operations, it speedily changes into the perfect insect.
But the beauty with which these little cells are formed transcends
conception. Each consists of a succession of layers of a membrane
more delicate than the thinnest goldbeater’s skin, and more lustrous
than the most beautiful satin. In glitter it most resembles the trail
left by the snail, and is evidently, from all experiments made, a
secretion of the insect elaborated from some special food it
consumes, and by means of its bilobated tongue, which it uses as a
trowel, it plasters with it the sides and the bottom of the tube it has
excavated to the extent necessary for one division. As this secretion
dries rapidly to a membrane it is succeeded by others, to the
number of three or four, which may be separated from each other by
careful manipulation. It then stores this cell, deposits the egg, and
proceeds to close it with a covercle of double the number of
membranes with which the sides are furnished, and continues with
another in a similar manner, until it has completed sufficient to fill
the tubular cavity, which, after closing the last case similarly to the
rest, it stops up the orifice with grains of sand or earth. The food
stored up is subject to fermentation, but this does not appear to be
prejudicial to the larva, which first consumes the liquid portion of the
store and then drills into the centre of the more solid part, and
continues enlarging this little cylinder until increasing in growth by
its consumption, it itself fills the cavity, and thus supplies the lateral
stay or prop which, by means of the stored provender, was
previously prevented from falling in. It has not been ascertained
what number of eggs each insect lays, or whether it bores more
than one tube, but it is presumable that it may do so, and possibly
thus, from the numbers annually produced, for there are two broods
in the year, colonies are thrown off which gradually form another
metropolis somewhere in the vicinity, although the majority continue
to occupy the old habitat from year to year. But the number of these
insects is kept within due limits by the individual abundance of the
parasites that infest them, and by the unsparing and unflinching
attacks of earwigs, which consume all before them,—perfect insect,
larva, and provender. The two most conspicuous parasites they
have, are the beautiful little bee, Epeolus variegatus, the young of
which is sustained, as in all bee-parasitism, by consuming the food
stored for the sustenance of the young of the Colletes; and the other
is the little dipterous Miltogramma punctata, whose larva, evolved
from the egg deposited in the cell, feeds upon the larva of the
Colletes, or possibly upon that of the Epeolus, which otherwise
would seem to have no check to its fertility, excepting that it may be
subdued by the Forficulæ.
These insects are to be found during the spring and summer
months, and throughout the southern counties, although some
species are extremely local. Some occur also in the north of England
and in Ireland. I am not prepared to say what flowers they prefer,
for I have never captured them on flowers, but they have been
found frequenting the Ragwort, and Curtis took a species at Parley
Heath, in Hampshire, on the Bluebell (Campanula glomerata). They
form a remarkable instance of an artisan bee, but so only in its
habits, amongst the Andrenides.

Two submarginal cells to the wings.

Genus 2. Prosopis, Fabricius.
(Plate I. fig. 2 ♂ ♀.)
Melitta * b, Kirby.—Hylæus, Latreille.
Gen. Char.: Head transverse, flattish; ocelli in an open triangle on
the vertex; antennæ geniculated, the basal joint of the flagellum as
long as the second, and both subclavate, the rest of the joints short
and equal; face flat, slightly protuberant between the insertion of
the antennæ, and distinguished from the clypeus by a suture;
clypeus transversely quadrate, slightly widening gradually to the
apex, marginate; labrum transverse, obovate, fringed with setæ;
mandibles broad at apex, tridentate; cibarial apparatus short; tongue
broad, subemarginate and fringed with short hair; paraglossæ very
slightly longer than the tongue, their apex broadly rounded and
fringed with hair; labial palpi as long as the tongue, joints subequal,
gradating in substance, subclavate; labium about as long as the
tongue, pyramidal at its apical inosculation; maxillæ about as long as
the tongue, slightly lanceolate, fringed with short hair; maxillary
palpi rather longer than the maxillæ, with six joints, the basal joint
robust and slightly constricted in the middle, the third joint linear
and the longest, the remainder gradually decreasing in length and
substance.