Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: enero-diciembre 2023 (Publicado Dic. 21, 2023)

BOOK REVIEW

Demystifying Orchid Pollination: back to the basics of Natural History

Karremans, A. P. (2023). Demystifying Orchid Pollination. Kew Publishing,

Royal Botanical Gardens, Kew, Richmond, Surrey, TW9 3AB UK, 440 pp.

Gerardo Avalos1, 2, 3; https://orcid.org/0000-0003-2663-4565

1. Escuela de Biología, Universidad de Costa Rica, 11501-2060 San Pedro, San José, Costa Rica; gerardo.avalos@ucr.ac.cr

2. The School for Field Studies, Center for Ecological Resilience Studies, 100 Cummings Center, Suite 534G, Beverly, MA

01915, USA.

Natural history is a multidisciplinary sci-

ence that combines evolutionary biology with

ecology and other fields, such as compara-

tive anatomy, paleontology, biogeography, and

biosystematics. Merging fields is essential to

understanding the patterns of distribution and

abundance of organisms, as this requires the

integration of evolutionary and ecological time.

The beauty of natural history lies in its multi-

disciplinary nature, which sets no boundaries to

scientific inquiry. This condition is fundamen-

tal in generating scientific knowledge through

the stimulation of human curiosity (Nanglu et

al., 2023). This emphasizes the importance of

natural history in knowing whether a question

is relevant and could be applied to a system, and

in calibrating experiments to hypothesis testing

(Travis, 2020). This process (a.k.a. the scien-

tific method) involves detailed observations,

hypotheses testing, developing experiments,

and collecting once again, more observations

and evidence. The ordered chaos of identify-

ing relevant questions and suitable systems

to answer them is far from being linear. Clas-

sic natural history is what emerges from the

pages of Adam Karremans’ book “Demystifying

Orchid Pollination”.

This book is a tour de force and a tes-

tament to the rich history of exploring the

mysteries of pollination focusing on the most

diverse Angiosperm family, Orchidaceae (with

over 30 000 species worldwide, Christenhusz &

Byng, 2016). Orchid flowers have a remarkable

complexity and intricate variations in morphol-

ogy and function, and thus, it is not surpris-

ing that they have captured the imagination

of naturalists since the beginning of civiliza-

tion. Demystifying Orchid Pollination shows

that Natural History, as a scientific method,

still has plenty to contribute to ecological and

evolutionary theory.

Karremans presents a very comprehen-

sive compilation of cases of orchid pollination

erroneously explained by myths. The subtitle

(Sex Stories, Lies and Obsession) could be inter-

preted, with some sarcasm, as synonymous

with pollination since it describes the nature

of the biological interactions that the pro-

cess involves, which includes deception, pollen

exchange and fertilization (sex), and many

times, the human obsession with sticking to

myths as simple but erroneous explanations of

phenomena with fragmentary evidence. Kar-

remans draws on classical natural history to

2Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: enero-diciembre 2023 (Publicado Dic. 21, 2023)

resolve these myths and crack the riddles of

orchid pollination. This involves gathering scat-

tered evidence through an exhaustive literature

review, conducting arduous and laborious field

observations and experiments, and consulting

with colleagues. Although this process may

seem simple, detailed observation of nature

requires great perseverance, patience, work

capacity, a detective mind… and yes, a consid-

erable number of hours in the field.

The book is organized into seven chapters.

Chapter 1 (Plot) provides the foundation and

starts with a summary of the history of research

on orchid pollination studies, then describes

orchid diversity and flower structure, and ends

with a revision of the discussion of pollina-

tion syndromes. Early naturalists focused on

describing the structure and anatomy of flower

parts rather than unraveling the ecological

mechanisms involved in pollination and fer-

tilization. Christian Konrad Sprengel (1750 to

1816) was the first to scientifically explore pol-

lination biology. His most significant contribu-

tion, The newly revealed mystery of nature in the

structure and fertilization of flowers, published

in 1793, was known by Charles Darwin and

certainly inspired his interest in orchids.

Since then, orchids have provided com-

pelling systems to explore evolutionary ques-

tions. Darwin was the first to describe in detail

reproductive strategies such as protandry in

terrestrial orchids and the production of imper-

fect flowers. He analyzed the causes of cross-

pollination and recognized its importance for

the evolution of species (Yim et al., 2009).

Additionally, Darwin demonstrated that flow-

ers had diverse strategies to attract pollinators,

and that many species avoid self-fertilization.

Darwin´s main contributions were the article

“Fertilization of Orchids” (1862) and the book

“The Various Contrivances by Which Orchids

Are Fertilized by Insects” (1862), dedicated to

the description of floral morphology and pol-

lination of orchids from temperate and tropi-

cal regions. In these works, Darwin showed a

laborious, precise, and specialized work where

he demonstrated how orchid flowers and their

pollinators matched in form and function

setting the stage and questions for future work

on orchids.

Also in chapter 1, Karremans pays hom-

age to the seminal works of Calaway Dodson

and Robert Dressler (researchers to whom the

book is dedicated). Dodson and Dressler made

significant contributions to the ecological, taxo-

nomic, and evolutionary knowledge of orchids.

Dodson and L. Van Der Pijl updated Darwin’s

book after a century with the book “Orchid

flowers: their pollination and evolution” (Van

Der Pijl & Dodson, 1966). The collaborations

of Dodson, Dressler, Van Der Pijl, and many

others, stimulated studies on orchid pollina-

tion, especially after the 1960s. However, the

field is still dominated by research on terrestrial

orchids, particularly those of temperate regions.

Despite their sheer diversity, tropical epiphytic

orchids have been little explored in terms of

their interactions with pollinators.

Chapters 2 (Deceit) and 3 (Reward) pro-

vide examples of species interactions and pres-

ent riddles, not only to pollination ecology but

to evolutionary biology. One can only speculate

how such intricate interactions between spe-

cies, as well as between groups of species shar-

ing phylogenetic relationships and common

pollinators, gave rise to coevolution and group

selection, guild mimetism, diffuse coevolution,

and other evolutionary mechanisms that are

just beginning to be explored. The evolutionary

origin of pollination relationships remains a

constant question throughout the book.

Chapter 2 deals with the many ways in

which orchids manipulate their pollinators

through deceit. In general, orchids have been

divided into those that provide rewards, and

those that deceive their pollinators, although

the difference is not obvious and there is con-

tinuous variation between both extremes as

reflected in the diverse assemblage of visitors

to orchid flowers. In the plant kingdom, the

Orchidaceae has the most species on record

with deceptive pollination mechanisms. In this

chapter, Karremans describes different pollina-

tion syndromes, from ornithophily, myophily,

myosaprophily, and psychophily. The concept

of syndrome refers to similar suites of flower

Revista de Biología Tropical, ISSN: 2215-2075, Vol. 71: enero-diciembre 2023 (Publicado Dic. 21, 2023)

traits found in evolutionarily unrelated taxa

that result from convergent selection by tar-

geting the same pollinating agent (Faegri &

van der Pijl, 1979; Dellinger, 2020). This may

sound like another oversimplification (another

myth?), but the concept has worked as a suit-

able model to establish patterns among groups,

both plants and pollinators, and Karremans

simply uses the term without entering the con-

troversy of whether it has been a useful concept

(Rosas-Guerrero et al., 2014). This chapter

provides compelling examples and spectacular

scenarios for the exploration of evolutionary

stable strategies. The book includes examples of

orchids that mimic the appearance of spiders to

deceive predatory and parasitoid wasps looking

for spiders, or orchids that generate an aroma

to attract male euglossine bees which will then

use it as a perfume to attract females, or orchids

that produce the scent of a fungus deceiving

flies looking for a reproductive site but that

then pollinate these orchids. The evolution of

these impressive strategies requires a fragile

balance between the frequency of deception

versus true rewards and the cleverness of the

flower visitor falling for the trick. For the trick

to work the frequency of the trickeries must be

lower than the negative impact on pollinator

fitness. The type of rewards is also very diverse

and vary from the absence of rewards and pol-

lination by deception, the presence of traces

of nectar that lure pollinators to visit flowers

without obtaining sufficient nectar, to flowers

whose aroma resembles rotting meat, which

offer both nectar and a sweet smell. One can

only wonder about the population dynamics

that must be at work for the evolution of these

deception strategies.

Three insect orders (Hymenoptera, Dip-

tera, and Lepidoptera) dominate orchid pol-

lination. Chapter 4 (Misfits) tackles the subject

of pollination misfits, this is, groups of pollina-

tors that do not fit the classic role of orchid

pollinators and include outliers such as beetles,

crickets, trips, and hummingbirds. Outliers

provide suitable systems to evaluate traditional

hypotheses on pollination biology.

Chapter 5 (Redesign) concentrates on the

variation of the pollination mechanisms, how-

ever, this adds to more bizarre cases of pol-

lination as an “improvement” of the already

not-so-regular cases, such as the mildly toxic

nectar of orchids of the genus Epipactis,

where wasps become drowsy after drinking

the toxic nectar and spend more time in the

flower doing erratic movements that eventually

accomplish pollination.

Chapter 6 (Fallacies) deals with even more

specific and often bizarre cases of interactions

around orchid flowers, such as lurking preda-

tors (called antipollinators) that use orchid

flowers as suitable sites for predation, or the

pseudo-antagonism interactions between male

bees and orchid flowers that mimic male bees

and are thus attacked by the males. It is not

clear in what instance the attack results in a

successful pollination. Karremans also tackles

some well-established myths about the high

specificity of pollinators, since most orchid

species do not have a well-documented fauna of

pollinators, and for those that do, high special-

ization is the exception.

Chapter 7 (Change) tackles the effect of

anthropogenic disturbances on orchid con-

servation. Being the most diverse angiosperm

family, it is not surprising that Orchidaceae

holds good and bad records, such as being the

family with the highest speciation rate but also

showing the highest extinction rate. Like most

organisms nowadays orchids are threatened

by anthropogenetic factors such as habitat loss

and fragmentation, over-collection, and climate

change, to name a few. Karremans discusses

the shifting seasons of pollinator emergence

vs blooming influenced by fluctuating tem-

peratures, whose lack of overlap is endangering

many pollination systems. Since habitat change

is a multifactor process the impact of climate

change on orchid pollination is understudied.

The book ends with a positive message foster-

ing the need to maintain biodiversity even in

the toughest places such as cities. Nature will

find a way.

4Revista de Biología Tropical, ISSN: 2215-2075 Vol. 71: enero-diciembre 2023 (Publicado Dic. 21, 2023)

Final remarks

The book highlights the crucial impor-

tance of fieldwork, which is evident from the

first pages but is especially clear in the accom-

panying videos. These are research videos, so

they do not feature fancy background music

or an entertaining narration. They are linked

to a QR code, which represents one of the

great contributions of the book as it becomes

a multimedia resource. The videos are excel-

lent at capturing pollinators at the right time to

illustrate a behavior and provide the evidence

needed to solve the puzzle of a particular

pollination mechanism. Technology can help

to resolve some myths around the pollina-

tion mechanism by amplifying the researcher’s

observation capacity, but it will not replace

scientific inquiry, which is stimulated by spend-

ing considerable time in the field. The book is

illustrated with beautiful photographs, which

not only fulfill the didactic objective of help-

ing to understand the text but also provide a

high-quality aesthetic element, which takes

place right from the beginning with the mag-

nificent book cover, evidence of the Lankester

the Botanical Gardens´ registered trademark of

excellence in nature photography.

The book is intended for a wide audience,

from biologists with specialized interests in

pollination biology to the public interested

in understanding orchid pollination and the

challenges it faces due to habitat loss, fragmen-

tation, and climate change. The book is filled

with specialized terms but is written in a very

accessible way relating topics peppered with

the titles of pop and rock songs. The reader

gets progressively acquainted with specialized

terms. In summary, Karremans´ book fills a

void in the natural history of orchid pollination

since Dodson and Dressler´s book. It highlights

the beauty of evolution maintaining a fragile

equilibrium between the conflicting interests

of plants and their pollinators and leaves many

questions to be resolved by population and

evolutionary biologists. As a pure, classic work

of natural history, Karremans’ book provides a

broad perspective on orchid diversity, pollina-

tion biology, and the resilience and adaptation

of natural systems.

REFERENCES

Christenhusz, M. J., & Byng, J. W. (2016). The number

of known plants species in the world and its annual

increase. Phytotaxa, 261(3), 201-217.

Dellinger, A. S. (2020). Pollination syndromes in the 21st

century: where do we stand and where may we go?

New Phytologist, 228(4), 1193-1213.

Faegri, K. van der Pijl (1979). The principles of pollination

ecology. Pergamon Press, Oxford, 113, 209-212.

Nanglu, K., de Carle, D., Cullen, T. M., Anderson, E. B.,

Arif, S., Castañeda, R. A., ... & Astudillo-Clavijo, V.

(2023). The nature of science: The fundamental role

of natural history in ecology, evolution, conserva-

tion, and education. Ecology and Evolution, 13(10),

e10621.

Pij, L. V. D., & Dodson, C. H. (1966). Orchid flowers: their

pollination and evolution (No. QK495. O64 P5).

Rosas-Guerrero, V., Aguilar, R., Martén-Rodríguez, S.,

Ashworth, L., Lopezaraiza-Mikel, M., Bastida, J. M.,

& Quesada, M. (2014). A quantitative review of polli-

nation syndromes: do floral traits predict effective

pollinators? Ecology Letters, 17(3), 388-400.

Travis, J. (2020). Where is natural history in ecological,

evolutionary, and behavioral science? The American

Naturalist, 196(1), 1–8.

Yam, T. W., Arditti, J., & Cameron, K. M. (2009). “The

orchids have been a splendid sport”—an alternative

look at Charles Darwin’s contribution to orchid bio-

logy. American Journal of Botany, 96(12), 2128-2154.