Spider Webs: Behavior, Function, and Evolution

By William Eberhard

In this lavishly illustrated, first-ever book on how spider webs are built, function, and evolved, William Eberhard provides a comprehensive overview of spider functional morphology and behavior related to web building, and of the surprising physical agility and mental abilities of orb weavers. For instance, one spider spins more than three precisely spaced, morphologically complex spiral attachments per second for up to fifteen minutes at a time. Spiders even adjust the mechanical properties of their famously strong silken lines to different parts of their webs and different environments, and make dramatic modifications in orb designs to adapt to available spaces. This extensive adaptive flexibility, involving decisions influenced by up to sixteen different cues, is unexpected in such small, supposedly simple animals.

As Eberhard reveals, the extraordinary diversity of webs includes ingenious solutions to gain access to prey in esoteric habitats, from blazing hot and shifting sand dunes (to capture ants) to the surfaces of tropical lakes (to capture water striders). Some webs are nets that are cast onto prey, while others form baskets into which the spider flicks prey. Some aerial webs are tramways used by spiders searching for chemical cues from their prey below, while others feature landing sites for flying insects and spiders where the spider then stalks its prey. In some webs, long trip lines are delicately sustained just above the ground by tiny rigid silk poles.

Stemming from the author’s more than five decades observing spider webs, this book will be the definitive reference for years to come.

• Language: English
• Publisher: University of Chicago Press
• Release date: Dec 22, 2020
• ISBN: 9780226534749

Book preview

Spider Webs

Spider Webs

Behavior, Function, and Evolution

William Eberhard

The University of Chicago Press

Chicago and London

Frontispiece: The recently discovered pseudo-orb of the New Guinean psechrid Fecenia ochracea is a spectacular example of a major theme of this book, evolutionary convergence. Although the spider is not closely related to the true orb weavers (Orbiculariae) its web shares with orbs a planar, aerial array of non-sticky radial lines that converge on a hub, frame lines that support the radii, and a uniformly spaced array of more or less circular sticky lines laid on the radii. The recent nature of this discovery, and the mystery of the ribbon-like nature of the sticky lines in the inner portion of the web (such band-like cribellum lines have never been described in any other species) emphasize a second general theme: our knowledge of spider webs (especially non-orb webs) is still profoundly incomplete (from Agnarsson et al. 2012; courtesy Ingi Agnarsson)

The University of Chicago Press, Chicago 60637

The University of Chicago Press, Ltd., London

Cover design and text design © 2020 The University of Chicago

All rights reserved. No copyright is claimed for the original text of Spider Webs: Behavior, Function, and Evolution, although some text and illustrations included in the book may be copyright protected.

For more information, contact the University of Chicago Press, 1427 E. 60th St., Chicago, IL 60637.

Published 2020

Printed in the United States of America

29 28 27 26 25 24 23 22 21 20 1 2 3 4 5

ISBN-13: 978-0-226-53460-2 (cloth)

ISBN-13: 978-0-226-53474-9 (e-book)

DOI: https://doi.org/10.7208/chicago/9780226534749.001.0001

Additional parts of this large project are archived online at press.uchicago.edu/sites/eberhard/; these portions are designated in the text with a capital O followed by the book chapter to which they refer (e.g., section O6.1; table O3.3; fig. O9.1).

Library of Congress Cataloging-in-Publication Data

Names: Eberhard, William G., author.

Title: Spider webs : behavior, function, and evolution / William Eberhard.

Description: Chicago : University of Chicago Press, 2020. | Includes bibliographical references and index.

Identifiers: LCCN 2019050065 | ISBN 9780226534602 (cloth) | ISBN 9780226534749 (ebook)

Subjects: LCSH: Spider webs. | Spiders—Behavior.

Classification: LCC QL458.4 .E24 2020 | DDC 595.4/4156—dc23

LC record available at https://lccn.loc.gov/2019050065

♾ This paper meets the requirements of ANSI/NISO Z39.48-1992 (Permanence of Paper).

To the memory of three great naturalists of web-building spiders:

REV. H. C. MCCOOK, MAJ. R. W. G. HINGSTON, and E. NIELSEN

A Noiseless patient spider

A noiseless, patient spider,

I mark’d, where, on a little promontory, it stood, isolated;

Mark’d how, to explore the vacant, vast surrounding,

It lauch’d forth filament, filament, filament, out of itself;

Ever unreeling them—ever tirelessly speeding them.

And you, O my Soul, where you stand,

Surrounded, surrounded, in measureless oceans of space,

Ceaselessly musing, venturing, throwing,—seeking spheres, to connect them;

Till the bridge you will need, be form’d—till the ductile anchor hold;

Till the gossamer thread you fling, catch somewhere, O my Soul.

—Walt Whitman

Contents

Chapter 1. Introduction

1.1 Introduction

1.2 A foreign world: life tied to silk lines

1.3 A brief history of spider web studies

1.4 Emphasis on behavior

1.5 The scope of this book and tactics in presentation

1.6 Evolutionary history and phylogeny

1.7 Terminology and other procedural matters

1.8 Acknowledgments

Chapter 2. The hardware of web-building spiders: morphology, silk, and behavior

2.1 Introduction

2.2 Silk glands and silk

2.2.1 Origins

2.2.2 Mechanical properties and how they are determined

2.2.3 Major ampullate glands

2.2.4 Minor ampullate glands

2.2.5 Aciniform glands

2.2.6 Flagelliform glands

2.2.7 Pseudoflagelliform glands

2.2.8 Sticky silk

2.2.8.1 Cribellum glands

2.2.8.2 Aggregate glands

2.2.8.3 Venom glands that produce contractile sticky webs in Scytodidae

2.2.8.4 Ampullate glands in Loxosceles

2.2.9 Piriform glands

2.2.9.1 Spinneret morphology

2.2.9.2 Morphology of attachment discs

2.2.9.3 Different attachment disc morphologies result from spinneret behavior and morphology

2.2.9.4 The piriform queen—Cyrtophora citricola

2.2.10 Epiandrous glands

2.2.11 Other products associated with silk

2.2.12 Control of rates of silk secretion in glands

2.2.13 Forming bridge lines

2.3 Spinnerets as high-precision instruments

2.3.1 Ancestral morphology and behavior

2.3.2 Strategic placements of spigots on the spinnerets of araneomorphs

2.3.2.1 General considerations

2.3.2.2 Special cases involving web designs

2.3.2.3 Additional complications

2.3.3 Phylogenetic inertia?

2.3.4 Behavior of the spinnerets

2.3.5 How are lines terminated?

2.4 Leg morphology and behavior: grasping lines precisely and securely

2.4.1 Grasping lines in a web; tarsal morphology and leg movements

2.4.2 Complementary searching and grasping behavior

2.4.2.1 The blind man’s cane and the art of following

2.4.2.2 Asymmetric searching movements that match asymmetric tarsal morphology

2.4.2.3 An additional detail: rotating legs to grasp lines

2.4.3 Grasping a line prior to attaching the dragline

2.5 Cutting lines and recycling silk

2.5.1 Cutting lines

2.5.2 Recycling silk

2.6 How spiders avoid adhering to their own webs: a mystery partly solved

2.7 Central nervous system basis for web construction

2.8 Summary

Chapter 3. Functions of orb web designs

3.1 Introduction

3.2 Correcting common misconceptions about orb webs

3.2.1 Orbs are neither sieves nor sound detectors

3.2.2 Orb webs are not the pinacle of web evolution

3.2.3 Orbs have never been demonstrated to be optimum structures

3.2.4 The trajectories, diameters, and velocities of prey are diverse and poorly known

3.2.5 Most differences in orb designs are probably not specializations for particular prey

3.2.5.1 Long lists of prey captured argue against strong specialization

3.2.5.2 Strong habitat effects

3.2.5.3 Data from prey counts generally have serious flaws

3.2.5.4 Measuring available prey is also difficult

3.2.5.5 Ontogenetic changes in web design (and lack of such changes) can introduce noise

3.2.5.6 Ecological settings of studies need to be evolutionarily realistic

3.2.5.7 Flexible construction behavior

3.2.5.8 Possible exceptions: relative prey specialization

3.2.5.9 A summary regarding prey specialization in orb webs

3.2.6 Interspecific competition for prey is probably not common

3.2.7 Sticky spiral spacing is not uniform

3.2.8 Orb designs are probably not taxon-specific

3.2.8.1 Species-specificity

3.2.8.2 Effects of intra-specific genetic differences

3.2.8.3 Genus-specificity?

3.2.8.4 Differences at higher taxonomic levels and a summary

3.2.9 The properties of homologous lines are not invariable

3.2.9.1 Differences between species

3.2.9.2 Differences within species

3.2.9.3 Consequences for understanding orb web designs

3.2.10 Correlations between orb design and details of attack behavior are inconsistent

3.2.10.1 Inconsistent relationships

3.2.10.2 More likely correlations

3.2.11 Orb movements in wind may not be generally significant in intercepting prey (but may affect orb designs)

3.2.11.1 Web movements and the encounter model

3.2.11.2 Different types of orb web movement in the wind

3.2.11.3 Orb movements in the wind: are they important?

3.2.11.3.1 Prey capture

3.2.11.3.2 Web damage

3.2.12 Prey are not defenseless: protection from the spider’s own prey

3.2.13 Design details are likely to be selectively important

3.2.14 Adultophilia: a serious arachnological problem

3.3 How orbs function

3.3.1 Intercepting prey

3.3.2 Functions for non-sticky lines (radii, hub and frame lines)

3.3.2.1 Stop prey

3.3.2.2 Transmit vibration cues for arousal and orientation

3.3.2.2.1 Longitudinal vibrations and their amplitudes

3.3.2.2.2 Precision of orientation and the importance (?) of radial organization

3.3.2.2.3 Types of prey vibration

3.3.2.3 Support the spider and facilitate her movements

3.3.2.4 Primary frame lines: adapt to variable spaces, increase extensibility, and avoid resonant vibrations (?)

3.3.2.4.1 Theoretical expectations of benefits and costs

3.3.2.4.2 Tests of predictions

3.3.2.5 Secondary and tertiary frame lines: increase extensibility

3.3.2.5.1 Tests of hypotheses

3.3.2.6 The hub: mechanical stabilizer, information center, and launching platform

3.3.2.6.1 Attack behavior and hub designs

3.3.2.6.2 Lines to pull, push against, and grasp while turning

3.3.2.6.3 Tensing (and relaxing) functions of the hub

3.3.2.7 Functions of the tertiary radii

3.3.2.8 Functions of the temporary spiral

3.3.2.8.1 Patterns in temporary spiral spacing

3.3.2.8.2 Probable functions of the temporary spiral (hand rail and others)

3.3.2.8.3 Patterns in temporary spiral spacing in orbs and their possible significance

3.3.2.9 The other side of the coin: how best to fail

3.3.3 Functions for sticky lines

3.3.3.1 Retain prey

3.3.3.1.1 Selection favors longer retention times

3.3.3.1.2 Means by which prey are retained: adhesion, extension, and resistance to breaking

3.3.3.1.3 Means of escape: prey behavior

3.3.3.1.4 Spaces between sticky lines

3.3.3.1.5 An orb’s slant

3.3.3.1.6 Pulley attachments of the sticky spiral to the radii

3.3.3.1.7 Variations in retention times and their consequences

3.3.3.1.8 Summary

3.3.3.2 Reduce the web’s visibility

3.3.3.2.1 Some insects can see orb webs

3.3.3.2.2 Does visibility affect prey capture in the field?

3.3.3.2.3 Yellow silk

3.3.3.3 Other functions

3.3.3.3.1 Survive environmental insults

3.3.3.3.2 Reduce construction costs and physical constraints

3.3.3.3.2.1 Behavioral costs?

3.3.3.3.2.1.1 Orb weavers

3.3.3.3.2.1.2 The special case of uloborids

3.3.3.3.2.2 Energetic constraints?

3.3.3.3.2.3 Material costs

3.3.3.3.2.4 The (unknown) costs of vigilance

3.3.3.3.3 Non-orb weavers

3.3.3.3.4 Defense against predators

3.3.3.3.5 Other possible variables and functions

3.3.3.4 Planar and non-planar orbs

3.3.4 The function(s) of stabilimenta

3.3.4.1 Egg sac and detritus stabilimenta

3.3.4.2 Silk stabilimenta

3.3.4.2.1 The hypotheses

3.3.4.2.2 Problems interpreting the data

3.3.4.2.2.1 Inconsistent support and behavior

3.3.4.2.2.2 Difficulties with direct measurements I: ecological realism

3.3.4.2.2.3 Direct measurements II: behavioral contexts, defensive behaviors, species differences

3.3.4.2.2.4 Direct measurements III: inappropriate measurements

3.3.4.2.2.5 The importance of UV reflectance

3.3.4.2.2.6 The hypotheses are not mutually exclusive

3.3.4.2.2.7 Some crucial behavioral phenomena are poorly understood

3.3.4.2.2.8 Comparing many apples with many oranges

3.3.4.2.2.9 Summary of weaknesses of direct measurements

3.3.4.2.3 Further complications: angles of view, illumination, and background

3.3.4.2.4 Conclusions

3.4 Summary

Chapter 4. Putting pieces together: tradeoffs and remaining puzzles

4.1 Introduction

4.2 Optimal orb designs: tradeoffs between functions are difficult to measure

4.2.1 Tradeoffs between functions

4.2.2 The rare large prey hypothesis: a dominant role for the stopping function?

4.2.3 Investments in foraging

4.2.4 Overview

4.3 Multiple trap design: a new way to view orb webs

4.3.1 Unequal spacing of radii is ubiquitous

4.3.2 Edge-to-hub patterns in sticky spiral spacing are also common—why?

4.3.2.1 Constraint by cues

4.3.2.2 Speed of attacks

4.3.2.3 Stopping prey

4.3.2.4 Sticky spiral entanglement

4.3.3 Illumination from exceptions

4.3.3.1 Low prey velocities

4.3.3.2 Tightly and widely spaced radii

4.3.3.3 Other patterns, other explanations

4.3.3.3.1 Above vs. below the hub

4.3.3.3.2 Inner edge of the capture zone, flimsy orbs, turnbacks

4.3.4 A limitation of current data: heterogeneity of lines

4.3.5 Conclusions regarding within-web patterns of sticky spiral spacing

4.3.6 Consequences for understanding how orbs function

4.4 Tensions and stresses

4.4.1 Theoretical expectations of uniformity in homologous lines are not confirmed

4.4.2 Tensions vary despite abilities to adjust them

4.4.2.1 Tensions on non-sticky lines in finished orbs

4.4.2.2 Different tensions along the length of a single radius

4.4.2.2.1 Web modifications that produce tension changes

4.4.2.2.2 Functions of altered tensions

4.4.2.3 Some spiders manipulate tensions in finished orbs

4.4.2.4 Tensions on sticky lines

4.4.2.5 Experimental manipulation of tensions

4.5 Relative numbers of radii and sticky spiral loops

4.6 Testing visibility and stopping functions: the extreme case of trunk orbs

4.7 Correlations between spider size and orb design?

4.8 Spider positions, attack behavior, and up-down asymmetries in orbs

4.8.1 Orb design and attack speed

4.8.2 Spider orientation at the hub

4.8.3 Further factors influencing spider positions at the hub

4.8.4 Summary

4.9 Remaining puzzles

4.9.1 The puzzle of temporary spiral removal

4.9.2 The puzzle of hub removal and open hubs

4.9.3 The puzzle of the free zone

4.9.4 The puzzle of non-vertical orbs

4.9.5 The puzzle of provisional radii

4.9.6 The puzzle of open sectors for detritus stabilimenta

4.9.7 Exceptions to trends

4.10 Non-orb webs

4.11 Evolutionary responses by insects? A neglected aspect of prey capture

4.11.1 Avoiding or reducing contact with webs

4.11.2 Reducing retention time after having been stopped by a web

4.11.3 Reducing the probability of being attacked immediately

4.12 Summary (including part of chapter 3)

Chapter 5. The building behavior of non-orb weavers

5.1 Introduction

5.2 Order of lines and other higher-level patterns

5.2.1 Modularity

5.2.2 Behavior deduced from patterns of lines

5.2.3 Other patterns

5.3 Lower-level patterns: leg movements and manipulation of lines

5.3.1 Walk upright on the substrate or a dense sheet

5.3.2 Walk under single lines

5.3.3 Hold the dragline while moving and while attaching it

5.3.4 Hold the line to which the dragline is being attached

5.3.5 Snub lines

5.3.6 Cutting and reconnecting lines

5.3.7 Finding lines and following behavior

5.3.8 Rubbing, brushing, lifting, and clapping movements of the spinnerets

5.3.9 Dabbing and sweeping with the entire abdomen

5.3.10 Other lower-level behavior patterns that are absent in orb weavers

5.4 Stereotyped behavior in non-orb construction

5.4.1 Building tunnels

5.5 Adjustments to substrate-imposed constraints

5.6 Managing swaths of fine lines

5.7 Summary

5.7.1 Higher levels of behavior

5.7.2 Lower levels of behavior

Box 5.1 The funnel web diplurid Linothele macrothelifera

Chapter 6. The building behavior of orb-weavers

6.1 Introduction

6.2 Simplifications for smoother reading

6.2.1 Species and topics

6.2.2 Levels of detail

6.3 Behavior of two araneids

6.3.1 Higher level organization: the stages of construction

6.3.2 Exploration and establishing early lines

6.3.2.1 Use previous lines or start from scratch?

6.3.2.2 Problems in starting from scratch

6.3.2.3 Basic operations during exploration

6.3.2.3.1 Gathering sensory information and laying the first lines

6.3.2.3.2 The end of exploration and the hub transition

6.3.3 Frames, secondary radii, and hub loops

6.3.3.1 The other primary frames

6.3.3.2 Secondary radii

6.3.3.3 Secondary frames

6.3.3.4 Hub loops

6.3.4 Temporary spiral and tertiary radii

6.3.5 Sticky spiral

6.3.5.1 Break temporary spiral lines

6.3.6 Modify the hub

6.3.7 Stabilimentum

6.3.8 Orb web repair

6.3.9 Web removal and recycling

6.4 Senility in orb construction: a new frontier?

6.5 Detailed movements

6.5.1 Patterns in variation: high diversity produces low diversity

6.5.2 Variation: a caution against stereotypy and typology

6.6 General patterns

6.6.1 Dexterity, the blind man’s cane, and following other legs

6.6.2 Patterns of tension changes during construction: a tendency to relax

6.6.3 Missing details

6.7 Summary

Chapter 7. Cues directing web construction behavior

7.1 Introduction

7.1.1 Building an orb in human terms

7.2 Classifying the cues

7.2.1 Stimuli from repeatedly sensed reference points vs. more nearly constant general settings

7.2.2 Other introductory notes

7.3 Cues for sticky spiral construction

7.3.1 Distinguishing sticky from non-sticky lines

7.3.2 Rapidly changing, repeatedly sensed reference point cues

7.3.2.1 Location of the inner loop

7.3.2.2 Distance from the outer loop of temporary spiral (TSP distance)

7.3.2.3 Memory of the TSP distance along the immediately preceding radius

7.3.2.4 Memory of less recent responses to changes in TSP distances

7.3.2.5 Distance between radii

7.3.2.6 Lack of influence of radius tension

7.3.2.7 Mistakes in discriminating sticky from non-sticky lines?

7.3.3 Intermediate, more slowly changing cues

7.3.3.1 Angle of the radius with gravity

7.3.3.2 Amount of silk available vs. web area

7.3.3.3 Distance from the hub (?)

7.3.4 More or less constant general settings

7.3.4.1 Length of the spider’s legs

7.3.4.2 Previous prey (escaped or captured)

7.3.4.2.1 General responses to prey

7.3.4.2.2 Prey-specific responses (?)

7.3.4.3 Presence of predators (?)

7.3.4.4 Wind

7.3.4.5 Time of day

7.3.4.6 Season of the year and light rain

7.3.4.7 Temperature

7.3.4.8 Humidity

7.3.5 Additional decisions by spiders building sticky spirals and cues triggering them

7.3.5.1 Turn back

7.3.5.2 Attach to each radius

7.3.5.3 Number of attachments

7.3.5.4 Break temporary spiral

7.3.5.5 Terminate

7.3.6 First loop of sticky spiral: a special case

7.3.7 Interactions among cues

7.4 Temporary spiral

7.4.1 Distances traveled and path integration

7.4.2 Gravity

7.4.3 Distance from the hub

7.4.4 Lack of effect of radius tension

7.4.5 Additional possible cues

7.5 Hub

7.5.1 Spaces between hub spiral loops

7.5.2 Termination of the hub spiral

7.6 Stabilimentum construction

7.6.1 Build a stabilimentum or not?

7.6.2 Where to place the stabilimentum?

7.6.3 Which stabilimentum design?

7.7 Radii, frames, and anchor lines

7.7.1 Secondary radii

7.7.1.1 Choosing an open sector

7.7.1.1.1 Radius length

7.7.1.1.2 False starts

7.7.1.2 Choosing an exit radius

7.7.1.3 Choosing a final angle: how far to move along the frame

7.7.2 Secondary frame construction

7.8 Early radii, and frames and anchor lines: determining web size, shape, and design

7.8.1 Position of the hub

7.8.2 Size and shape of the space in which to build

7.8.2.1 The decisions the spider makes

7.8.2.2 The cues used in decisions

7.8.3 Spider size and weight

7.8.4 Silk available in the glands

7.9 To build or not to build: triggering orb construction and destruction

7.10 Cues that trigger transitions between stages of orb construction

7.11 Other stimuli that spiders can sense but that are not (yet) known to guide orb construction

7.11.1 Tensions

7.11.2 Handedness?

7.12 Hints of abilities: follow circular paths and sense radius lengths

7.13 Effects of psychotropic drugs on orb construction

7.14 Coordinating different adjustments to different cues

7.15 The (limited) role of simulations in understanding orb construction behavior

7.16 A missing link: translating cues into attachment sites

7.17 Summarizing the behavioral challenges met by orb weavers

7.17.1 Mechanical agility and precision

7.17.2 Analytical abilities: multiple cues and decisions

7.17.3 Sustained attention—where orb weavers truly shine

7.18 Independence (?) of the spider’s responses

7.19 Changes in responses to cues: learning and maturation

7.20 Cues guiding the construction of non-orbs

7.20.1 Path integration

7.20.2 Smooth substrates for gumfoot lines

7.20.3 Rigidity of supports

7.20.4 Locations of supporting objects

7.20.5 Radial symmetry

7.20.6 Differences in tensions

7.20.7 Temperature

7.20.8 Apparent sensory movements of legs

7.20.9 Reserves from previous feeding

7.20.10 Conspecifics (gregarious and social species) and possible constraints imposed by orbs on sociality

7.20.11 Web repair

7.21 Summary

7.21.1 Surprising patterns in orb construction, especially sticky spiral construction

7.21.2 Other stages of construction

7.21.3 Non-orb webs

Chapter 8. Web ecology and website selection

8.1 Introduction: what is and is not included

8.2 Webs and ecological foraging theories

8.3 What is enough? Fast lane and slow lane spiders

8.4 Processes that produce habitat biases

8.4.1 Searching with lines floated on the breeze

8.4.2 Sensory biases: satisficing and special problems for aerial webs

8.4.3 Biases in choosing websites

8.4.3.1 Philopatry—remain near the natal web

8.4.3.2 Disperse and then settle selectively—possible cues

8.4.3.2.1 Problems quantifying websites in the field

8.4.3.2.1.1 Website choice in simple field situations

8.4.3.2.1.2 Experimental evidence

8.4.3.2.2 Rigidity, spacing, and surface characteristics of supports

8.4.3.2.3 Temperature

8.4.3.2.4 Egg sacs and retreats

8.4.3.2.5 Light—artificial and otherwise

8.4.3.2.6 The presence of prey

8.4.3.2.7 Preexisting webs

8.4.3.2.8 Isolation

8.4.3.2.9 The presence of predators

8.4.3.2.10 Humidity

8.4.3.2.11 Plant species

8.4.3.2.12 Wind and other factors that may bias insect movements

8.4.3.2.13 Height above the ground

8.4.3.2.14 Food quality and satiation

8.4.3.2.15 Season of the year

8.4.3.2.16 Possibility of damage (?)

8.4.3.2.17 Ant nests

8.5 A general correlation between website selectivity and web design flexibility?

8.5.1 Post-building selectivity and cues

8.5.1.1 Prey capture success

8.5.1.2 Learning how to adjust

8.5.1.3 Web damage

8.5.1.4 Material fatigue in silk lines?

8.5.1.5 Kleptoparasites

8.5.1.6 Pilot webs—a risk-minimizing tactic

8.6 Website tenacity, web durability, and recycling

8.7 Web durability

8.8 Limited by websites? Possible competition for prey and websites

8.8.1 Inter-specific competition

8.8.2 Intra-specific competition

8.9 Problems in attempts to study cues that guide website choices

8.9.1 Experimental tests need controls: how to count unoccupied sites?

8.9.2 Measuring habitat richness: sticky traps do NOT mimic spider webs

8.10 Time of day: day webs vs. night webs

8.10.1 Multiple orbs in a single day

8.11 Summary

Chapter 9. Evolutionary patterns: an ancient success that produced high diversity and rampant convergence

9.1 Introduction

9.2 Patterns in the diversity of webs

9.2.1 High diversity

9.2.2 Frequent convergence

9.2.3 Abundant intermediate forms and a summary

9.2.4 Intra-specific alternative web designs

9.2.5 Behavioral bricks and buildings

9.2.6 Adaptive chemical diversity of silk

9.2.7 Differences between conspecifics: are there individual styles of web design?

9.3 Consequences of the failure of the prey specialist hypothesis for understanding diversity and convergence

9.4 What is a sheet web? Problems inherited from previous imprecision

9.5 Mygalomorphs: similar patterns of diversity and rampant convergence in a different world

9.6 Diversity of relations with insects

9.7 Lack of miniaturization effects

9.8 Paths not followed: alternative web forms in other animals

9.9 Summary and a new synthesis

Box 9.1 The most spectacular convergence of all: Fecenia

Box 9.2 The most spectacular divergence of all: Theridiidae

Box 9.3 Sand castles: extreme modifications of Seothyra henscheli webs to shifting sand

Box 9.4 Relation between web design and silk properties: stiff silk in Uroctea durandi

Chapter 10. Ontogeny, modularity, and the evolution of web building

10.1 Introduction

10.2 Web ontogeny and evolution

10.2.1 Limits of interpretations

10.2.2 A new hypothesis for ontogenic changes: consistent selection associated with smaller size

10.3 Early web evolution

10.3.1 Burrow entrances vs. egg sacs

10.3.2 Interception function for earliest webs

10.3.3 Retention function in early webs

10.3.4 Webs without retreats in the substrate

10.3.4.1 Independence from the substrate is not a qualitative trait

10.3.5 Sheets with sticky lines and tangles

10.3.6 Early-branching araneomorph lineages with derived webs

10.3.7 Spider webs and insect flight

10.3.8 Summary

10.4 The behavior patterns used to build early webs

10.4.1 Male sperm webs, burrow closures, and the origin of prey capture webs

10.4.2 Moving upside down below silk lines

10.4.3 Using legs to manipulate lines

10.4.4 Managing swaths of fine lines

10.4.5 Diplurid behavior: a possible guide to ancestral traits

10.5 Evolution of later non-orb webs

10.5.1 Consequences of cribellum silk loss in labidognaths

10.5.2 Problems categorizing web types in evolution

10.5.3 Problems with key innovation arguments in general

10.5.4 Silk glands and other morphological traits

10.5.5 Visibility of silk to prey

10.5.6 Web evolution in two small groups

10.5.6.1 Filistatid webs

10.5.6.2 Interception vs. retention in oecobiid webs

10.6 Inconsistent evolutionary trends in non-orb webs

10.7 Diversity in non-orbs that results from behavioral stability

10.8 The (probably) monophyletic origin of orb webs

10.8.1 Evolutionary origins when behavior is modular

10.8.2 Morphology, molecules, and behavior

10.8.3 Fossils and possible precursor webs

10.8.4 Speculations on the origins and consequences of cut and reel behavior (and the possible role of males)

10.8.5 Derivation of ecribellate sticky lines from cribellate sticky lines

10.8.6 Summary regarding orb monophyly

10.9 Evolutionary changes in orb designs

10.9.1. Horizontal vs. vertical and nearly vertical orbs

10.9.2 Small derived lineages: ladder and trunk webs

10.9.3 Derivation of deinopid webs

10.9.4 Theridiosomatids and their allies

10.9.5 The reduced webs of Hyptiotes and Miagrammopes

10.9.6 Twig orbs: an object projects through the hub

10.10 Post-orb web evolution in Orbiculariae

10.10.1 Possible derivation of other web types from orbs

10.10.1.1 Gumfoot webs

10.10.1.2 Other web types

10.10.2 Webs combined with prey attractants

10.11 Coevolution between attack behavior and web design (and its lack)

10.12 What didn’t happen, possible synapomorphies, and further puzzles

10.13 Modularity and adaptive flexibility

10.13.1 Modularity is a central pattern in web construction

10.13.1.1 Direct observations of behavior

10.13.1.2 Finished structures

10.13.1.3 Ontogenetic and experimentally induced changes

10.13.1.4 Summary

10.14 Modules and evolutionary transitions in web-building behavior

10.14.1 Use of web construction behavior in taxonomy

10.14.1.1 Historical successes and failures

10.14.1.2 Implications of modularity for orb monophyly

10.15 Summary

References

Index

1

Introduction

1.1 Introduction

This book is about how spider webs are built, and how and why they have evolved their many different forms. It was conceived during a field trip in a spider biology course, when a student asked me why I had not written a book on spider webs. She noted that such a book would have been useful for the course but did not exist. She was right on both counts, and also that I was well-placed to produce it. I am an evolutionary biologist particularly interested in behavior. I have had the great fortune of living most of my working life in the tropics, and have spent just over 50 years watching a diverse array of spiders and thinking about their webs. Writing this book represents a chance both to contribute general summaries of data and ideas that are currently lacking, and to organize and develop new ideas that grew out of producing these summaries.

Inevitably, the book’s coverage is idiosyncratic. I propose more new ideas, give more new data, and discuss more extensively those topics related to behavior and evolution; some discussions in other areas, like the biochemistry and mechanics of silk, are more standard and less original. I focus on behavior and evolution partly because spider webs have the potential to make especially important contributions to resolving central questions in behavior and evolution, just as they did in the past in understanding the characteristic and limits of innate behavior (Fabre 1912, Hingston 1929). An orb web can be easily photographed with perfect precision, and it constitutes an accurate record of a series of behavioral decisions made by a free-ranging animal under natural conditions. And because a web-building spider’s sensory world is so centered on silk lines, the orb is also a precise record of some of the most important stimuli that the spider used to guide those decisions; in addition, these stimuli can be experimentally altered by making simple modifications of webs. These advantages offer unusual chances to study some basic questions in animal behavior with especially fine detail and precision.

I hope that this book may help future observers to see how web-building spiders can be exploited to investigate exciting new questions in animal behavior. It is a fragment of a larger project that originally included several additional topics: the role of behavioral canalization and errors in the evolution of behavior; the importance of scaling problems in the absolute and relative brain sizes of tiny animals and the limitations in behavioral capabilities that they may impose; the organization and evolution of independent behavior units in the nervous system; the implications of chemical manipulations performed by parasitoid wasps on their spider hosts and of additional experimental manipulations of webs for how behavioral subunits are organized and controlled in the spider; and the possibility that small invertebrates understand, at least to some limited degree, the physical consequences of their actions and the role that such understanding may play in the evolution of new behavior patterns. Other fragments of this larger project are archived online at the University of Chicago Press at press.uchicago.edu/sites/eberhard/; these portions are designated in the text with a capital O followed by the book chapter to which they refer (e.g., section O6.1; table O3.3; fig. O9.1). My hope is that this book will help to project the study of spider webs back onto the forefront of studies of animal behavior.

1.2 A foreign world: life tied to silk lines

Spiders are ecologically extremely important: for instance, a recent estimate suggests that they capture 400–800 million metric tons of prey each year, or about 1% of global terrestrial net primary production (Nyffeler and Birkhofer 2017). Web spiders live in a world that is ruled by their silk lines. This world is so different from ours, with respect both to their sensory impressions and to the basic facts of what is and what is not feasible for them to do, and they have such exquisite adaptations to this world, that it is useful to briefly describe these differences here, anticipating more detailed descriptions in later chapters (references documenting these statements will be given later). My aim is to help give the reader the kinds of intuition that are needed to understand their behavior.

Orb weavers are functionally blind with respect to their web lines. Their eyes are neither designed nor positioned correctly to resolve fine objects like their lines, and in any case many spiders build their webs at night. Watching an orb weaver waving her legs as she moves is thus like watching a blind man use his cane, with two differences: the spider is usually limited to moving along only the lines she has laid (and thus has to use her canes to search for each new foothold); and the lines are in three rather than two dimensions. Slow motion recordings reveal a further level of elegance. Spiders economize on searching as they walk through a web; one leg often carefully passes the line that it has grasped to the next leg back on the same side before moving on to search for the next line. Each more posterior leg needs to make only a quick, small searching movement in the vicinity of the point that is being grasped by the leg just ahead of it.

This dominance of the sense of touch gives observations of orb weaver behavior a dimension that is largely missing in many other animals, because the spider’s intentions can be intuited from the movements of her legs. One can deduce a blind man’s intentions by watching the movements of his cane; when he taps toward the left just after he hears a sudden growling sound from that direction, he is probably wondering about the origin of that sound. And it is also clear what he has found out; if his cane has not yet touched the dog that growled, he probably does not yet know its precise location. The searching movements that a spider’s legs make to find lines, especially at moments during orb web construction, when one can predict the next operations that she will perform, make it possible to confidently deduce both her intentions and the information that she has perceived. For instance, when the orb weaver Leucauge mariana is moving back toward the hub after attaching the first radial line to a primary frame while she is building a secondary frame (when she is at approximately the site of the head of the inward arrow from point p in fig. 6.5j), she consistently begins to tap laterally with her anterior legs on the side toward the adjacent radius (o in fig. 6.5j) that she is about to use as an exit to reach the second primary frame. The movements and their timing leave no doubt about what she is attempting to do: she is searching for the adjacent radius. In some cases it is possible to deduce, even in a finished web, what the spider may or may not have sensed at particular moments during the web’s construction by taking into account leg lengths and the distances between lines. This access to both the intentions and the information that an animal has (or lacks) offers special advantages in studies of animal behavior.

An orb weaver is also largely chained to its own lines. In one sense, the spider lives a life similar to that of a blind person who is constrained to move only along preexisting train tracks. And just like a blind man walks around and taps objects in a room to sense its size and the presence or absence of furniture in it, the spider searching for a site in which to build a web must explore it physically, rather than surveying it visually. Much of this exploration must occur by following lines that were already laid previously; the spider cannot simply set out in any arbitrary direction. While spiders sometimes lay new lines by walking along a branch or a leaf and attaching the dragline line, at other times the only way for the spider to lay a new line from one distant point to another is by floating a line on a breeze and waiting until it snags somewhere. The spider has no control over the strength or direction of the wind, nor how or where the line snags. If the line fails to snag firmly on a useful support object, the spider’s only recourse is discard it and try again. To evaluate a possible website (is it too large? too small? does it have a projecting branch that would interfere with a web?), the spider probably remembers the distances and directions she has moved while exploring it (sections 6.3.2, 7.8).

Fig. 1.1. Three outstanding observers of spider webs and building behavior from the late nineteenth and early twentieth century (left to right): Rev. Henry C. McCook, Major R. W. G. Hingston, and Emil Nielsen (the last two courtesy of, respectively, Royal Geographic Society, and Nicolas Scharff).

And then there is the web itself. Orbs are famously strong, and able to resist both the general loads imposed by wind and the local stresses from high-energy prey impacts. But they are also foreign to some human intuitions. The lines are extremely light, and because air is relatively viscous at the scale of a small animal like a spider, transverse vibrations that would dominate a web at a human scale are strongly damped in spider webs. A more appropriate image is an orb of flexible lines strung under water. Not unexpectedly, spiders rely mainly on longitudinal rather than transverse vibrations of their lines to sense prey and other spiders. And while an orb is strong, it is also delicate in unexpected ways. A few drops of rain, a fog, or even dew can be enough to ruin it: the sticky spiral lines adhere to each other, the radii, and the frame lines, and the sticky material on the lines of most species washes off in water. Wind can cause individual sticky lines to flutter and become damaged when they swing into contact with each other. Some patterns in sticky spiral spacing in orbs may represent adaptations to reduce this type of damage (section 3.2.11).

In sum, web-building spiders live a life that is limited by their own senses, and tightly bound to the silken lines in their webs. To understand these spiders, it is necessary to understand their webs, and vice versa.

1.3 A brief history of spider web studies

Spider webs are, of course, common and easily observed. The history of scientific inquiry regarding webs and spider building behavior begins, as with that of many other fields in biology, with descriptions by field naturalists. Important early works, now difficult to obtain and which I have not read, included Quatremére-Disjonval 1792, 1795, Reimarus and Reimarus 1798, Blackwall 1835, Dahl 1885, and Wagner 1894. The American clergyman H. C. McCook (Fig. 1.1) (in addition to providing distinguished service in the American Civil War and writing popular children’s books on insects, religion, and leaf cutter ants) described many details of natural history and behavior in unprecedented detail (McCook 1889). The nineteenth-century giant of spider taxonomy, Eugene Simon, also contributed scattered but precise observations of webs (Simon 1892–1903). Also important, with acute observations and the first collections of good photographs of webs, were the books of Emerton (1902), Comstock (originally published in 1912, revised in 1967), and Fabre (1912).

Somewhat later, perhaps the two best naturalist observers of spider orb webs and of building behavior were the Irish medical doctor and explorer Maj. R. W. G. Hingston (Hingston 1920, 1929, 1932) and the Danish school teacher Emil Nielsen (Nielsen 1932) (Fig. 1.1). Hingston parlayed military assignments in India, Pakistan, and Iraq, and subsequent expeditions to British Guyana and other sites, into opportunities to observe tropical spiders (and other animals) and describe their behavior. His careful observations of the details of web construction, his incisive simple experiments, and his thoughtful analyses are particularly striking in light of his energetic physical undertakings, which included participation in an expedition to climb Mount Everest and scaling tropical trees to collect specimens on the trunks and in the canopy. The other giant contrasted in many ways. Emil Nielsen was a Danish secondary school teacher who did not travel to exotic places to study spiders, but instead made thorough, careful comparative studies of web-building spiders in Denmark. He published an especially thorough book-length study in Danish and, mercifully for English-speakers, combined it with a condensed companion volume in English (Nielsen 1932). Nielsen’s work on the parasitoid wasps that induce changes in the web-building behavior of their host spiders was also exceptionally thorough and insightful. Both Hingston and Fabre discussed general questions regarding instinctual behavior and the limits of the mental and behavioral capabilities of invertebrates, comparing them with other animals and humans.

Other especially important general studies in the field of webs and their diversity were those by Herman Wiehle (1927, 1928, 1929, 1931) in northern Europe and the Mediterranean, Hans Peters (1931, 1936, 1937, 1939, 1953, 1954, 1955) in Germany, the Mediterranean, and tropical America, and B. J. and M. Marples in Europe and Oceania (Marples and Marples 1937; Marples 1955). Additional laboratory studies of orb web construction behavior during this and the following generation mostly centered on two European araneids, Araneus diadematus and Zygiella x-notata (e.g., Peters 1931, 1936, 1937, 1939; Tilquin 1942; König 1951; Mayer 1952; Jacobi-Kleemann 1953; Witt 1963; Le Guelte 1966, 1968; Witt et al. 1968), and the American uloborid Uloborus diversus (Eberhard 1971a, 1972a). Studies of the webs of isolated species continued, and began to include more tropical species (e.g., Robinson and Robinson 1971, 1972, 1973a, 1975, 1976a).

Up to about 1960, one might say that the history of spider web studies was pretty typical of many topics in zoology. Kaston (1964) presented a pre-cladistic hypothesis concerning spider web evolution, based almost entirely on observations of North temperate zone species. But long after the time had seemingly come for a detailed general, in-depth summary of what was known about webs and construction behavior, it was still missing. Theodore Savory produced a short general popular book (Savory 1952) with an admirable tendency to emphasize general questions, but with many undocumented and sometimes imprecise statements. Peter Witt, Charles Reed, and David Peakall wrote a more scholarly book (Witt et al. 1968), but it was limited almost entirely to laboratory observations of two species, Araneus diadematus and Zygiella x-notata. An important summary published 24 years later continued this unfortunate tradition, specifically omitting data on any species other than A. diadematus (Vollrath 1992). Ernst Kullmann published large numbers of beautiful photographs of the webs of many heretofore unstudied species (Kullmann 1971/1972, 1975; Kullmann and Stern 1981) but did not produce a general overview. An edited book (Shear 1986) provided detailed and thorough summaries of some aspects of the webs and building behavior in particular groups (e.g., Coyle 1986; Lubin 1986) and included a brief summary (Shear 1986), but there was no synthetic, in-depth overview. A more recent general, synthetic book (Craig 2003) emphasized chemical and physical properties of silk, rather than behavior, but was unfortunately largely confined to summarizing the author’s own studies (Vollrath 2003; Higgins 2004).

A few large, general papers and chapters giving overviews of webs and building behavior have appeared recently. Some have emphasized their use as taxonomic characters (Griswold et al. 2005; Kuntner et al. 2008a) and have tended to ignore function. Others give more general reviews (Viera et al. 2007; Blackledge et al. 2009c, 2011; Harmer et al. 2011; Herberstein and Tso 2011) but have been necessarily incomplete, especially with respect to behavior and to web designs other than orbs. A thorough, book-length review of spider webs, and of their functions and construction behavior, has yet to be written. This book attempts to fill that niche.

The lack of a general summary on spider webs is having unfortunate consequences. Several aspects of the current academic environment favor neglect of older work: the relatively greater ease of obtaining electronic copies of more recent as opposed to old papers; the widespread emphasis in hiring and promotion decisions on quantity rather than quality of publications; and trends that favor claims to originality over thorough historical research and integration of new data with prior knowledge. Some recent papers on spider web biology have carried the modern trend of neglecting previous work to new heights (or depths), either lacking relevant citations of earlier literature, or simply citing one or two recent papers or a review to cover all other previous work. Here are four examples. The clear leader in the field of orb web construction biology in the 1950s and 1960s was Peter Witt; yet three large recent reviews cited only 3, 1, and 0 of his publications. Only one of these three reviews even cited the two old but revolutionary papers, Riechert and Cady (1983) and Wise and Barata (1983), that up-ended most previous attempts to relate web designs to inter-specific competition and the kinds of prey that they capture. In a squabble over whether one group of spiders (theridiids) are capable of the highly coordinated movements that are used in the specialized cut and reel behavior (Fig. 6.3) (Benjamin and Zschokke 2002, 2003, 2004; Eberhard et al. 2008a), none of the authors cited the clear, complete older descriptions of this behavior in theridiids (Marples 1955; Bradoo 1972). And none of several recent major reviews of the vexed problem of stabilimentum function even cited the 1932 book of Hingston, in which he devoted 60 full pages to stabilimenta in tropical species.

I believe there is a real danger that much earlier knowledge is being lost. A comprehensive summary may be more important in spider webs than in some other fields. I have thus attempted to minimize citing only recent summaries (which, of course, are often less than complete, and sometimes include imprecise or even erroneous interpretations of previous work). I have made a special effort to be more complete with non-orb webs, because they have been less-studied, and show some previously unrecognized patterns (e.g., Figs. 1.2, 1.3).

Nevertheless, I am certain that I have not covered the sprawling published literature completely. In the best of all possible worlds, with the best of all possible minds and memories, and fluency in other languages (especially German and Japanese), I would have liked to have rendered this service. But I have no illusions of having made a truly thorough review (in any case, it would make very dull reading). I find that even when I read papers a second or third time, I routinely find additional important points that I missed previously; I have had quite different interests and ideas in my head at different stages of this project. My review of recent literature tailed off in late 2016. The MS was delivered to the press in August 2017, and after that I mostly only completed in press citations as they were published. I apologize in advance to all the authors whose work I cited only partially or missed completely, and warn the reader of this limitation.

I have also added bits of unpublished information that I have accumulated during nearly 50 years of observing spiders and their webs (cited as WE). One result of writing this book was to make me aware of many lacunae in our current knowledge, and the book has launched me on several projects along the way that were designed to fill some of these holes. Several species that are abundant where I live, including the filistatid Kukulcania hibernalis, the araneid Micrathena duodecimspinosa, the tetragnathid Leucauge mariana, and the uloborid Zosis geniculata are thus over-represented in the text. I have also pointed out many remaining gaps in our understanding, and compiled outstanding questions and promising research topics, in the online Table O10.1 in the hope that this will be useful to future researchers.

1.4 Emphasis on behavior

The emphases here on behavior and behavioral evolution come naturally. Orb web construction behavior has long been considered an iconic example of stereotyped innate behavior, and details of orb construction behavior provide especially valuable traits for higher-level taxonomy (Eberhard 1982; Kuntner et al. 2008a). In addition, orbs offer unusually favorable conditions for studying behavior at especially fine levels of detail and precision and testing general ideas (Ades 1986). This is because an orb web is an exquisitely precise, detailed record of many aspects of the spider’s construction behavior (Fig. 1.4). Both the animal’s behavior and some of the crucial stimuli that were used to guide that behavior are frozen in the pattern of lines in the web (Zschokke and Vollrath 1995a). Behavioral decisions are easily recorded in photographs, because orbs are generally two-dimensional. In addition, the spider is guided largely by the positions of other web lines as she builds, especially during temporary spiral and sticky spiral construction, so many of the stimuli that guide her behavior can be deduced from web photos (chapter 7). Other possible stimuli from the web that would be more difficult to quantify from photographs, such as tensions and patterns of vibrations, appear not to provide important stimuli, at least during the latter stages of web construction (section 7.3.2.6). Instead, orb construction is probably largely guided by aspects of an orb such as distances and angles between lines and that can be measured precisely in photos. The precision with which both potential stimuli from an orb web and the spider’s behavioral responses can be measured is something that behaviorists studying most other animals can only dream about. And these fine analyses can be conducted on behavior that was performed in the natural context of building its web, rather than some highly constrained or artificial situation.

Fig. 1.2. Beautiful complexity and diversity is not limited to orbs, as illustrated by the aerial sheet webs of the linyphiids Frontinella sp. (a), Labulla thoracica (b), and Tapinopa bilineata (c). The F. sp. web had an unusually tall knock-down tangle above the dense horizontal sheet where the spider rested, a nearly clear space just below where a few lines pulled the sheet sharply downward into a cup, and a sparse tangle with a hint of a planar structure below this which may have served to protect the spider from predators. The naked horizontal sheet of L. thoracica (b) lacked tangles; it had a retreat at one edge (arrow) and a more open mesh near the edges. The T. bilineata sheet (c) also lacked tangles, but seen from the side it proved to be a double sheet loosely joined at the edge, forming a cavity that enclosed the spider (photographs by Gustavo Hormiga).

Fig. 1.3. This sampler illustrates some kinds of organization that are as yet only poorly documented in non-orb webs of mature females, including lines radiating from the spider’s retreat (dashed arrow) in a linyphiid sheet web (Agyneta sp.) (a), zig-zag sticky lines centered on a retreat (dashed arrow) in a desid web (Matachia livor) (b), and skeletons of long, more or less straight lines (arrows) that support the sheet webs and extended beyond some edges in the pisaurid Architis sp. (whose web is unusual in having two, approximately vertical sheets, connected by a short tunnel) (c), and the pholcid Modisimus bribri (d) (see also fig. 5.21). The zig-zag sticky lines (strong white lines) in the web of M. livor imply two patterns seen in the construction behavior of many non-orb spiders. The sticky lines must have been built after the non-sticky lines (or at least those between which the zig-zags are built). And construction of the sticky lines, must have occurred in discrete bouts in different sectors of the web. Web construction behavior has never been observed directly in this species (or in any other desid), so these inferences remain unconfirmed (a photograph by Gustavo Hormiga, b courtesy of Brent Opell).

Orb weavers also offer additional practical advantages for a behaviorist. Because of the limitations of the spider’s sensory world and the great importance of stimuli from the lines in the web in guiding her building behavior, simple experimental manipulations of these lines can reveal how they guide the spider. With only moderate care, it is possible to observe a spider closely without alarming it. Spiders tend to build their webs at highly predictable sites and times, and construction behavior often involves many highly repetitive behavior patterns, allowing an observer in the field to observe fine behavioral details over and over, and eventually understand them. Repetition also offers unusual opportunities to evaluate the frequency with which spiders make errors and examine the conditions which promote errors (section 9.7), difficult topics that are presently uncommon in studies of animal behavior but which may be important in understanding how behavior evolves (Eberhard 1990a, 2000a). While these advantages are especially clear in orb webs, non-orbs also offer scope (which has hardly been exploited) for deductions about behavior (Fig. 1.4), including how behavior is organized and the effects that this organization has on behavioral evolution and the mental processes involved in compensating for previous errors (Figs. 5.3, 5.4). Variability is the rule in orbs, even when sequential webs are built by the same individual at exactly the same site (e.g., Fig. 7.41).

In sum, I believe that orb web construction behavior can be in the vanguard as studies of animal behavior move past the current, largely typological stage (focused on the behavior of a species), and on to population thinking in which variation and its consequences are described and analyzed (Mayr 1982). For instance, orb webs permit one to employ huge sample sizes to study the sizes and frequencies of true behavioral errors (section 9.7) and possible lapses of attention (Eberhard and Hesselberg 2012), as well as variation in adaptive flexibility in behavior (which in most species has also been treated typologically, such as the behavior that is performed under condition x, and the behavior under condition y). Another consequence of the frozen behavior is to facilitate study of the multiple influences on the same decision. For instance, ten or more different variables influence each decision that an orb weaver makes when she attaches a loop of sticky spiral to a radius (section 7.20.1). While the behavioral record offered by an orb is incomplete (for instance, more than one type of leg movement can produce a particular web design) (Vollrath 1992), combining observations of webs with observations of the building behavior itself can nevertheless provide a very unusual opportunity to study behavior in great detail. One objective of this book is to provide a solid base on which a new generation of behavioral studies can be built.

Such mechanistic details, which used to be standard fare in animal behavior studies, are currently out of style; many recent studies of behavior emphasize instead ultimate causes—the effects of natural selection on behavior in terms of reproductive payoffs. Sooner or later, however, behaviorists will have to return to the study of behavioral mechanisms in order to understand how selection actually brings about its effects on behavior; in the end, the mechanisms are the traits on which selection acts. The field of morphological evolution has already entered this sort of transition, with a rebirth of interest in the previously neglected effects of developmental processes (Nijhout 1991; Raff 1996; West-Eberhard 2003).

Orb web spiders have often been thought of as small automatons that are tightly programmed to build the same species-specific webs day after day, and that are completely unconscious of their own work (Fabre 1912; Hingston 1920, 1929). It is true that spiders need no previous learning to produce an orb, and indeed, spiderlings that have just emerged from the egg sac can spin complete webs on their first try (Fig. 1.5); and there is little indication that their behavior improves with practice (section 7.19). As described long ago by Hingston (1920), spiders seem unable to make even what would seem to be simple adjustments to some experimental alterations to their webs: Introduce difficulties in its circuit . . . , build up obstructions to impede the blind routine, and the spider can do nothing to overcome them; it can only struggle in its course. It can appreciate none of these difficulties; it can understand none of these obstacles; all it can do is but circle on (p. 134).

Fig. 1.4. This orb of a mature female Micrathena duodecimspinosa illustrates both the beautiful geometric regularity for which orb webs are famous, and subtle patterns of irregularity. The graph below shows that although the spaces between the loops of sticky spiral are highly regular, those nearer the outer edges are considerably larger than those nearer the hub (except for the innermost few loops below the hub). This pattern, common in the orbs of several families (Eberhard 2014; see fig. 3.6), leads to the proposal that an orb should be viewed not as a single unit prey trap, but rather as a combination of traps with different prey-catching properties in different portions of the orb (section 4.3). To give an idea of scale, this web of an approximately 1 cm long spider, contains the following: 18.7 m of sticky spiral; 9.6 m of radii (including the set of radii that she broke and reeled up, then later reingested when she removed the center of the hub); 0.4 m of hub loops; 1.6 m of frame lines; and 1.5 m of anchor lines. It has 3840 attachments (319 of non-sticky lines to each other, 3521 of sticky to non-sticky lines). Not bad for about 40 min of work.

Fig. 1.5. This was the first orb web built by a spiderling of the nephilid Nephila clavipes after emerging from the egg sac; it illustrates an additional pair of themes of this book—the apparently minor role of learning in web construction behavior, and the blind spot of adultophilic arachnologists. The black dots indicate intact loops of the non-sticky temporary spiral, an unusual trait that is present in this first orb of the spider’s life just as in the orbs of adults (see fig. 4.4). The small tangle in the foreground (which obscures the spider resting at the hub) is another unusual trait also found in adult webs. The web’s highly regular design and its similarity to the orbs of mature females show that these spiders need little or no learning to build an orb. The basic similarity between the orb designs of young spiderlings and adults, typical of most orb weavers, is also striking in view of the differences in their sizes: the spiderling weighed on the order of 1 mg, while adult females weighed on the order of 1000 mg. They must confront very different ecological problems such as distributions of prey sizes and abundances, possible websites, predators, and parasites. Arachnologists studying web designs have traditionally analyzed the costs and benefits of orb designs for the adult, and neglected the behavior and ecology of younger stages. This adultophilic bias needs to be overcome, because selection must act on web designs throughout a spider’s life (see section 3.2.14).

This simple automaton view has gradually eroded, however (see summaries in Herberstein and Heiling 1999; Herberstein and Tso 2011; Hesselberg 2015), and one of the themes in this book is that it must now be discarded. Spiders clearly show substantial, multi-dimensional flexibility in their web construction behavior (see, for example, Figs. 1.6, 6.2, 7.36). It is possible that these adjustments may themselves result from pre-wired alternative behavior patterns, implying that the appropriate change in views is from a simple to a complex automaton. It is also possible, however, that spiders have some sort of primitive understanding of the mechanical consequences of their building behavior (Eberhard 2019b).

The original impression of simplicity and invariability that was associated with the early oversimplified descriptions of orb construction behavior has been followed by a gradual accumulation of exceptions to the behavioral rules, and an appreciation of previously unnoticed or unreported subtlety and variations. This process is incomplete, and our present understanding is undoubtedly still overly typological. In addition, there is obviously much still to be learned, even about well-studied species (Fig. 1.7). The need to deal with such variation has increased the difficulty of writing this book. I have struggled to avoid two extremes: overly simplistic descriptions of behavior and webs that are clear and easy to understand but seriously underestimate variation; and overly complex descriptions that are more nearly correct but are too convoluted for even the most motivated reader to follow.

Fig. 1.6. These webs illustrate the behavioral flexibility of orb weavers, a major theme of this book. The two webs built in captivity by Philoponella oweni (UL) (a-c) illustrate alternative phenotypes: a is a complete horizontal orb with no tangle; b and c show a tangle web seen from above. In b all lines in the web are visible, while in c only the sticky lines are visible (the web was coated with white powder and photographed in b, and then jarred repeatedly to remove the powder from all non-sticky lines and photographed again in c). Other webs of this species included both an orb and a tangle; some individual spiders built all three web types. A second type of flexibility (d), in which spiders adapt their web designs to the environments in which they find themselves, is illustrated by the horizontal web of an immature Tetragnatha sp. on a strand of barbed wire (the elongate spider was hidden under the wire at the hub).

1.5 The scope of this book and tactics in presentation

A great deal is known about spider webs, and in order to avoid an incomprehensible sprawl of endless lists, I have often emphasized only more general trends and ideas, attempting to avoid giving so much detail that the reader loses view of the most interesting aspects of the forest for the trees. Much detailed data is relegated to tables and online appendices. So much is now known about spider webs that a truly thorough summary of current knowledge would be crushingly dull. I have tried to make the text accessible to a general reader by focusing on particular illustrative examples rather than making exhaustive discussions, and by filling in some details with extensive figure captions. In many places I have avoided giving long strings of citations to document a particular statement, citing instead another section of the book where previous work on the topic is discussed more thoroughly.

I have attempted to evaluate previous studies critically, because there is both imprecision and controversy in some published accounts. Presenting convincing and fair discussions of conflicting ideas sometimes posed a challenge, because the data and the arguments were complex and tedious. Nevertheless I wanted to avoid two tactics that are unfortunately common in recent publications: simply accepting all published claims at face value; or dismissing (or even ignoring) some views without giving any justifications. These traits can make for smooth prose, but are unfair to both readers and previous authors. Advances in science often depend on disproving hypotheses, so the reasons for discarding previous ideas are important (Popper 1970). And some imprecise ideas, if not specifically challenged, acquire lives of their own when they are repeated uncritically by subsequent authors. In a few, particularly complex topics I give only simplified discussions in the text, and detailed critical discussions in appendices. Even this tactic has its limits (there is simply not enough room, for instance, for a thorough discussion of every single function that imaginative arachnologists have proposed for the function of silk stabilimenta) (see section 3.3.4).

Fig. 1.7. A serious historical problem in spider webs studies has been the tendency to use typological descriptions of web designs that overlooked details and variations. This kind of problem is illustrated in these images of webs of Cyrtophora citricola (AR), whose general design was described nearly 100 years ago (Wiehle 1928) and has subsequently been studied extensively (Blanke 1972, 1975; Kullmann 1972; Lubin 1973, 1974, 1980; Sabath et al. 1974; Berry 1987; Peters 1993a; Rao and Poyyamoli 2001). Nevertheless, several previously under-appreciated details reveal further sophistication of these webs as traps. Early descriptions mentioned a dense tangle of lines above and below a horizontal, planar sheet (see a, a largely finished, 4-day old web), and a clear organization of the lines in the sheet, with frequently bifurcating radial lines that converged on a central hub that were connected by an uniformly spaced, tight non-sticky spiral. The tangles above and below the sheet were said be connected to its outer edges, and also, in the case of the upper tangle, to the hub. But closer examination adds several details. An image of this same web after only a single night of building (b; in this image, in contrast with the others, the web was not dusted), shows that the tangle was built by stages. The spider first built only a sparse