Promoting the In-Depth Understanding of All Forms of Life

Life: The Excitement of Biology

Promoting the in-depth understanding of all forms of life

Volume 2 of 2014

Blay Publishers LLC York, Pennsylvania, USA

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Printed on acid-free paper in York, Pennsylvania, USA Life: The Excitement of Biology 2(1) 1

The first year of Life: The Excitement of Biology

Jorge A. Santiago-Blay1

Back in March 2013, when I began putting together the first issue of Life: The Excitement of Biology, I did not know that I would be writing again, at the beginning of another spring after such a harsh winter in eastern USA, with one volume containing four issues and over 250 printed pages under my belt. Herein, now feeling a peaceful sense of accomplishment and having volume 1 behind, I have a little time to reflect on that first year. LEB 1(1) brought a lot of joy into my life, as I imagine the first newborn does for willing parents. That issue was completed on time and it nearly met most of my expectations. Circumstances beyond my control made the next two issues, LEB 1(2) and LEB 1(3), just as LEB 2(1), not go as smoothly as I had planned. However, the expeditious inclusion of LEB by prestigious indexing units, such as Biosis, Biological Abstracts, and CAB Abstracts, gave me an energy boost for a larger and LEB 1(4), published on time. The diversity of biological topics and authors speaks volumes concerning the kind of mix I welcome in LEB. The generosity of many colleagues and friends made my desire to be kind, fair, and humble, while trying to provide fast service, easier. Members of the boards of Life: The Excitement of Biology provided timely advice on numerous occasions. While juggling the responsibilities of a researcher, a faculty member, along with my editorial duties, I have had the privilege of communicating with numerous authors, reviewers, subscribers, who have expressed their strong support of this effort. They have offered many constructive suggestions, including something obvious that I forgot on LEB 1(1): an inside title page. Ms. Meghan Frost (Metapress, Birmingham, Alabama) and the Courtright Family of York, Pennsylvania, owners of NeFra or “the printers”, have always been willing to help with the almost unavoidable last minute issues, too numerous to recount. To all of them, my wholehearted thanks. Please, feel free to spread the word about LEB and its high quality, fast publication, and helpfulness; a great value, in sum, science for all. I hope all of you join me in a wonderful voyage of discovery during 2014.

Peace and wellness, sincerely and gratefully,

Jorge Santiago-Blay, Ph.D. Editor-in-Chief, Life: The Excitement of Biology, http://blaypublishers.com/

1 217 Wynwood Road, York, Pennsylvania 17402 USA. E-mail: [email protected]

DOI: 10.9784/LEB2(1)Santiago-Blay.01 Electronically available on May 16, 2014. Mailed on May 14, 2014. Life: The Excitement of Biology 2(1) 2

The Anthropological Consumption of Non-Human Primates, the Other Black Meat1

Reniel Rodríguez Ramos2

Abstract: The other has been the main staple consumed by the anthropological enterprise. One of the most succulent others consumed by anthropology has been the non-human primates. This work discusses the anthropological construction of primatological alterity as a tool for colonizing subaltern beings and peoples, using as heuristic mechanisms the temporalization of space and the naturalization of the other.

Key Words: Non-human primates, alterity, revisionist primatology, postcolonial anthropology

Anthropology has made its livelihood the construction of the other, since its main agenda has been to create a notion of the Western self based on its distinction from the rest of the creatures, both human and non-human (Haraway 1985, 2003, 2008). This “anthropophagous” discipline (Islam 2012) devised its otherness scale using as its baseline white male adults from Western societies to which the rest of humanity and the animal world has been weighed against to determine their degree of otherhood. One of these others used in anthropology has been the non-human primates (NHP), and their study has served a similar function in anthropology as non-Western (principally hunter-gather and other “traditional”) societies, being both considered as subjects that provide indications of our pristine hominid state as well as our natural behavioral and organizational structure. In this sense, anthropologists have treated NHP as another “culture” created by an anthropologically motivated ethnogenetic process. Thus, similar parameters as those traditionally employed to create, study, and categorize other human cultures have also been applied to primates to justify the uniqueness of western humans within the natural and the cultural order. This has resulted in the concomitant cultural anthropologists’ focus on “traditional” subalterns like the !Kung San of the Kalahari or the Mbuti of the Congo with the emphasis of anthropological primatologists to study other “ primate cultures” such as the chimpanzees (Pan spp.), gorillas (Gorilla spp.), and orangutans (Pongo spp.), among others. Perceptions about what constitutes the other in anthropology have been defined along two major domains, which are not necessarily mutually exclusive: time (present/past) and space (the east/west dichotomy) (Fabian 1983). At the

1 Received on April 23, 2014. Accepted on April 27, 2014. Last revisions received on May 5, 2014. 2 Associate Professor, Programa de Ciencias Sociales, Universidad de Puerto Rico, Recinto de Utuado, Utuado, Puerto Rico 00641-2500. E-mail: [email protected]

DOI: 10.9784/LEB2(1)Rodriguez.01 Electronically available on May 16, 2014. Mailed on May 14, 2014.

Life: The Excitement of Biology 2(1) 3

same time, other dualistic relationships have been tied up in this discourse: the black/white divide and the nature/culture metaphysic (Figure 1). These hierarchical and politically charged dichotomies have been used by anthropology since the start of the discipline as a tool of power, as one of the elements which has characterized it has been its ingrained colonialist conception of the domination of western (white-self) over non-western (black-other) societies and, in the same light, the supremacy of culture (West-self) over nature (non-Western-other) (Haraway 1978a, 1989). It is within this context that the politics involved in the study of non-human primates in anthropology were articulated and, with some fortunate variations, has persisted until this day. Unfortunately, however, those human and non-human that constitute the subject of study of anthropology have not necessarily received much benefit from the unsolicited intrusion into their lifeways, and thus in many cases the impact that these receive from these interventions has commonly outweighed the scientific retribution that has been gained from getting to know them to better know ourselves, as is clearly reflected by the sad example of Ota Benga which was at the core of the development of anthropology as a discipline (McCray 2012).

Figure 1. Temporalization and naturalization of the “other”. Image modified from http://www.doeaccimphal.org.in/m18/file.php/1/final%20contents/56/index.html; text added by the author. Life: The Excitement of Biology 2(1) 4

In this paper, I explore the metaphorical construction of non-human primates analogous to non-western cultures in anthropological discourse, and establish the uses and abuses to which these anthropological objects, as well as the rest of the “primitive” world, have been subjected within the discipline to through the use of temporalization and naturalization devises that have served to justify their consumption. It should be noted that I write this from the perspective of an archaeologist born and raised in an “eccentric context” (Pagán Jiménez 2004; Pagán Jiménez and Rodríguez Ramos 2008), who understands that in many ways the history of those creatures that inhabit nature mirrors that of us who still live in colonized territories, those who have been the meat consumed by the anthropological enterprise.

The Temporalization of the Other Our modern conceptualization of time have had marked repercussions in the ways that anthropology has constructed the non-Western human and “animal” world. Modern concepts of secular time consider it as dimension that progress along a unidirectional, cumulative, and lineal axis (Bailey 1983). This vertical perception of progress through time has traditionally been tilted horizontally, thus leading to the equation of time with distance from the West and thus from “culture,” resulting in the temporalization of space (Fabian 1983). In this sense, time was (and still is) used as a distancing device in the anthropological construction and classification of alterity, or otherness, which became the subject of study of the discipline since its onset. The spatio-temporal construction of alterity has been used by anthropologists to position the West with respect to the other, which also led to its manipulation as a tool to legitimize the colonialist enterprise that characterized the development of the discipline since its beginnings (Gosden 2004). Time is power and it has served as a control mechanism used to order non-Western peoples through the construction of their histories and in the justification for the exploitation of nature for enhancing our progress as the dominant species in the natural order (Fabian 1983). This time perspectivism has also been translated in the construction of the “savage slot” (Trouillot 2003) as something old, and thus of the natural world as an entity that reflects the pristine conditions in which our early hominid ancestors lived. This progressive notion of time was related to the rise of evolutionary thought in anthropology in the first part of the 20th century, in which views of NHP became tied with the articulation of a narrative of our progress along a unidirectional evolutionary vector which gradually separated us from the rest of those soulless creatures, as well as from the savages that inhabited the recondite jungle space. In this respect, NHP have been employed in a similar fashion as those other “primitive” cultures, as a “central iconography of the human past” (Sperling 1991:1), since they provide information of the ways of life of our hominid ancestors and of the innate structure that governs Life: The Excitement of Biology 2(1) 5

some of our behaviors. Louis Leakey used this perspective as one of the justifications for conducting studies on primates when he handpicked Biruté Galdikas-Bridanmour, Dian Fossey, and Jane Goodall to study orangutan, gorillas, and chimpanzees respectively. As noted by Hinde (1978:1; emphasis mine), who was Jane Goodall’s dissertation chairman, the study of NHP would “not only help us gain a deeper understanding of Man himself and his origins, but also understand how and why he is like he is today.” Thus, at the onset of the discipline, especially after World War II, primate data was used in anthropology to understand the biological substratum that could condition some of our behaviors (Marcus 1990). Primatology was employed initially in anthropology in its physical subfield by concentrating on conducting morphological comparisons between NHP and the fossil hominid record in order to determine the ubiquity of physical parallelisms between the embryonic “us” and “them” (Schultz 1955). Later, the study of primates was fomented in order to explore their behaviors, which might help us gain a better understanding of those first chapters of the evolution of “Man” (Hinde 1978). More recently, studies on NHP as well as on other “simple” or “traditional” societies are still being focused on the reconstruction of human origins, using as tools theoretical frameworks such as behavioral ecology and sociobiology (e.g. Rodman 1999). However, as has been noted in revisionist hunter-gather literature and historical anthropology, the use of NHP and “traditional” societies for modeling our past behaviors and natural structure has been based partly on the uniformitarian assumption that both of those analogs have not gone through any formation processes that have characterized the Western world and thus represent fossilized stages of evolution (i.e., Pompeii premise; Murray 1999). The selection of NHP and other “traditional” cultures as relevant analogies are primarily based on a typological notion of the chronos (Fabian 1983) in which space and time are merged into a single domain in order to illustrate our past living conditions and the laws that regulate our behaviors on the basis of the purported similarity of similar stages of evolution between them and our fossilized ancestors (Dunnell 1982). In this sense, the main emphasis has been placed on the synchronic relationship between analogous units rather than on their particular historical developments (Stahl 1993). This, however, has been considered by some to be totally misguided as it is now widely known that most of the “traditional” societies and NHP that are used as analogs have history, as these have gone through considerable transformations due to internal causes, and the marked environmental changes that have occurred over the millennia thus limiting their adequacy for reconstructing our human past (Stahl 1993). So, the notion of an unchanging nature used to justify the employment of NHP and “traditional” societies for modeling our evolutionary development and the structure of our present needs to be considered in more detail, as both of these have had a history which needs to be taken into consideration since it might be Life: The Excitement of Biology 2(1) 6

critical for, not only sorting out their alterations through time, but also for enhancing their survival in the future. The artificial distance that was and still is created with this human and nonhuman other has also led to the view that the more distant from the anima urbis (Wolf 2002) the more natural, and thus older, it becomes. Thus, as will be noted in the next section, time becomes nature that becomes the other along a single, lineal vector.

The Naturalization of the Other The spatio-temporal distance created between us and the human and non- human other that has been used in anthropology to justify them as subjects of study, has been partly based on creation of a “scientific” boundary between culture and nature. The construction of nature as the other’s space has been used to facilitate the scientific classification of its inhabitants into the ordered taxonomies of “natural” categories used in the definition of non-Western cultures as well as the different types of NHP (Khalidi 1998). As previously noted, our construction of what is “natural” and thus what might be treated as other has been intimately related to the artificial temporal distance that has been created with nature. This separation, however, is almost inexistent for most other people who live in intimate relation with nature, who have long recognized the crosscutting relationship that we have with the rest of the creatures that inhabit in this planet (Lizarralde 2002). Despite this, such distance needs to be maintained in the anthropological discourse to justify the study of these others due to the basic subject-object dichotomy that is quasi-required in most of the scientific frameworks used today. Not only the objective definition of who the other is, but also the delimitation of the space in which that other exists have also been naturalized in order to justify the imposition of Western cultural domination. Anthropology, and later primatology, was originally based on work conducted in non-Western countries, some of which were also the subject of the colonialist enterprise carried out by emerging empires, which were expanding their political and economic supremacy to extraneous terrains (Gosden 2004). These spaces outside the comforts of what used to be called the “First World” were culturally envisioned through a “darkening mirror” (Batiste 2012), depicting them as obscure (black) places full of chaos, mystery, and danger (i.e., “it’s a jungle out there”). The nonhuman and non-Western human’s world was treated as a big natural zoo where the beasts were uncaged and the people who lived there were envisioned as hordes of “faceless blobs” (Tringham 1991). In these spaces, the images of the Western explorers that went either to study the primitives (anthropologists), to study ruins of human’s past (archaeologists), or to capture the creatures that lived in such world (western hunters) were basically indistinguishable from one another, and thus a public parallel was established between the different kaki-clothed “adventurers” (all compressed in the image of Life: The Excitement of Biology 2(1) 7

Indiana Jones) with the study of the primitive, dark, unknown, and dangerous. These were the spaces and the creatures that were to be understood to be conquered (i.e. consumed), and thus formed the basis for the anthropological enterprise. The anthropological conception of the “natural” as a space to be conquered through its understanding (i.e., “what we don’t know can hurt us”) remained pivotal in the discipline. However, it began to be problematized in the anthropological arena in part with the advent of the feminist critique, which focused on the domination of the female body and its social manipulation for control purposes. This has led to the questioning of our view of the embodiment and engendering of the “natural” and the justifications that have been devised to legitimize its exploitation (Harraway 1978a, 1978b; Keane and Posergarten 2002). In this refiguring of the biological, feminist scholars have tried to unsettle the nature/culture divide and have looked at how such dichotomized relationship has been used to naturalize the social discourses, based on anthropologically derived “scientific” criteria, that justified the asymmetrical relations of power between the sexes and between the West (culture) and nature (non-Western contexts). As noted by Sperling (1991), with the use of data derived from studies on NHP male dominance became reasonable in its natural aim to organize and control women and the subaltern, as it formed part of their natural structure. In this sense, women became “nature,” and their body became a space that was to be conquered, controlled, and exploited. The engendering of nature as a space that can be dominated in a similar fashion as men have done (or tried to do) with women in most societies, has been considered by some to be one of the possible reasons for which some of the most famous representatives of this field are females. Perhaps, as noted by Harraway (1985:490), Leakey’s selection of women for doing the fieldwork was due to the idea that “women’s place is in the jungle,” and while men went to conquer it women went to nurture its creatures (Fedigan 1994). This public perception of the nurturing woman primatologist is still highly pervasive, and perhaps might explain why Julia Roberts (instead of George Clooney) was sent to Borneo’s jungle in order to care for some of its endangered creatures in the “documentary” The Animal Mind. And, interestingly enough, the number of women primatologists is on the rise. According to the figures of the American Society of Primatology (Shapiro 2003), around 58 percent of primatologists that are part of that association are women, and that number seems to be on a steady climb if we consider that of the 110 degrees given in primate-related studies in the last two decades of the last century, 90 (75 percent) were awarded to women, most of them graduated with terminal degrees in Anthropology. Furthermore, the current board of directors of the American Society of Primatologists (2012- 2014) is composed exclusively of females. Whether this represents a subconscious reproduction of the previous conceptions of woman, the caretaker, Life: The Excitement of Biology 2(1) 8

as noted by Fedigan (1994) or is indicative of other gender-related factor deserves further scrutiny (Adessi et al. 2012).

The Consumption of the Other The previously noted cannibalistic tendencies of anthropology have also entailed the naturalization of the other as a tool for facilitating its consumption, since the farther away that something is from culture the more natural it is and thus the more edible it becomes. The process of naturalizing the colonization of the other might be observed in different fashions. One of the main ways in which the West has canned the natural in order to consume it has been in the development of public displays of our human power over nature of which the most evident are the zoos. In these microcosms of the Noah’s arc an attempt is made, not only to have a representative sample of those wild creatures which inhabit the dark spaces of nature, but also to demonstrate how we have the power to control its creatures by encasing them into squared prisons. This has been most eloquently expressed by Wolf (2002:723), who noted that in the construction of Australia’s Adelaide Zoo “zoo practices consolidated and legitimated Australian colonial identity, naturalized colonial rule and oppression of indigenous peoples, and reinforced gendered and racialized biases of human- animal boundaries.” These confinement spaces for animals have not only been used as displays of human power over nature, but also as images of the boundaries that humans have with the non-human and of our capacity of domesticating the other for our own benefits (Harraway 1985). The construction of zoos and the continuous search for animals for filling their cages have been justified primarily because of the educational role they play (Anderson 1995). However, the use of these spaces of animal suffering based on educational purposes is not justified, especially when we take into consideration that what zoos actually portray are creatures living outside their natural contexts, behaving in many cases in aberrant ways, walking in circles as if they were trying to dig their graves with their own steps. I agree with Gooding et al. (1997:27) that “we must return them all to their natural environments” with the necessary provisions, in order to provide them back their “sovereignty.” Another form of encapsulating nature has been the creation of National Primate Research Centers (Shapiro 2003). One of the earliest of these was created in Cayo Santiago, a small island off eastern of Puerto Rico. There, in the 1930’s Clarence R. Carpenter set free around 400 rhesus macaques to analyze the ways in which these reorganized “naturally” in a new environment and the typical behaviors that developed in such situations. Interestingly enough, this led these monkeys to organize hierarchically by competitive aggression and, as noted by Harraway (1978b) and Sperling (1991), these similar attributes were later used to scientifically legitimize the beliefs of the Life: The Excitement of Biology 2(1) 9

naturalness of male dominance over women and of the aggressive appropriation and consumption of the other. This caging of the other has not only been used for the non-human world but also for some of those “primitives” that live in the non-Western world. The most famous of these was the case of Ishi, the last Yahi survivor, who was brought by Berkeley anthropologists to a San Francisco museum and was put into display to demonstrate his primitive capacities of stone tool making, until he died of tuberculosis in 1916. This creation of a view of “animality” in the other was an intrinsic part of the development of anthropology and its use by the colonial powers to gain possession of their new territories (i.e., nature) and their inhabitants (i.e., animals) (Mullin 1999). In fact, when looked in these terms, the indigenous populations of most Western countries have been encased in limited territories defined as “reservations” which might be best regarded as “anthrozoos.” Another way of consuming the NHP other has been in their use in biomedical research, exploiting their bodies for exploring ways of mitigating imperfections in our biological design. This is another instance that reflects the discourse of colonization of nature and the human-based justifications that are devised in order to legitimize it. In fact, this use of the other as lab rats is in no way much different from the use of Puerto Rican women to test fertility pills in the 1960’s (without knowing that they were being forming part of an experiment) by the United States government, which led to death of at least a dozen of them and the permanent infertility of many others. The use of biomedical research using the other as the subject of study also provides another interesting instance that shows how the condition of alterity is manipulated in order to justify its exploitation. No case is clearer than that related to the transplantation of non-human organic matter (organs, blood, or cells) to humans (i.e. xenotransplantation). At the onset of medical experiments on this practice, NHP were the first to suffer their dismemberment to determine if their parts were fit to fix human medical problems due to the fact that these were the most comparable animals to us, although paradoxically the scientific promoters of this practice defended their technology by noting that they were still different enough from us to justify their consumption (Brown and Michael 2001). However, a public shift in opinion to one that advocated for a more intimate human (i.e., genetic and “cultural”) relationship to NHP led to their later exclusion for their use for transplants because “they would be exposed to too much suffering” according to the Advisory Group on Ethics of Xenotransplantation (Keane and Ponsengarten 2002:272). Interestingly enough, they replaced NHP meat with that of the pig, “the other white meat,” since no one would claim allegiance to the porcine lineage, but their organs were argued to be similar enough to ours to justify their medical consumption. This emphasis on studying the other, in this case the NHP, for extracting biological capital to benefit ourselves is evident in the figures on the distribution Life: The Excitement of Biology 2(1) 10

of fields of study of primates provided by the American Society of Primatologists, which indicate that the vast majority (around 85 percent) of its active members are working in issues dealing with behavior, cognition, and communication (the last two being a minority), while only 15 percent of the people working in that field are actually engaged in any activity related to the conservation of those species (Shapiro 2003).

Concluding Remarks As previously noted, anthropology has made use of the data generated from NHP in a similar fashion to that derived from the study of “traditional” societies: to better define the Western self by contrasting it to the other. As noted by Haraway (1978b:37), “we polish an animal mirror to look at ourselves,” and that has been precisely the primary goal of anthropology and its use of primatology in the past. Anthropologists and primatologists continue to argue about the boundaries between humans and the rest of the natural order, while at the same time they are often trespassing the other’s boundary without their consent (Rees 2001). In trying to justify the incorporation of studies of NHP more deeply into the anthropological arena, Kinzey (1986) asked the questions of, what’s in it for Anthropology? Unfortunately, there does not seem to be a proportional amount of people asking, what’s in it for the other?

Acknowledgements I want to thank Sue Boinski for motivating me to write this article. Thanks also to two anonymous reviewers for their comments. This material is based upon work supported under a National Science Foundation Graduate Research Fellowship.

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Ontology Confounds Reproducibility in Ecology and Climate Science1

Brent Wilson2 and Lee-Ann C. Hayek3

Abstract: The ability to reproduce ecological or climate change experiments or quantitative results is a hallmark of science, but not the only one. In addition, a scientist who subsequently examines original research must be able to reproduce the interpretation of the observations. Confidence in both ecology and climate science research is undermined when an a priori interpretation cannot be confirmed. This will happen when an a priori (before investigation) assumption was introduced by the original author(s), even inadvertently, regarding the nature of the universe or a subset of it. Such an assumption is here termed an ontological assumption when it then is treated as invariant; that is, it is not changed as unsupportive evidence, whether positive or negative, is accumulated. It thus conditions the interpretation of observed scientific phenomena. The results of the scientific investigation are therefore interpreted within the framework of this assumption, even though this framework is at variance with actual results obtained. Recent decades have seen increasing use of paleoclimatic studies as predictors of what will happen as current global climate change unfolds. Here we consider how the results from impact studies of paleoclimatic change on biotic communities have been used as a basis for neoclimatic and ecological research and prediction. We show that in some cases at least the observed results of these paleoclimatic studies were not in accord with the original interpretations, the paleoclimatic workers having held onto unwarranted ontological assumptions in the face of observations to the contrary. This practice is a threat to validity and undermines the applicability of these original paleonvironmental studies to later neoenvironmental work. For example, contrary to expectations, Pleistocene glacial-interglacial cycles did not always impact on community diversity, whether measured by species richness or the information function. Likewise, the quantitative assemblage turnover index (ATI) shows that in the greenhouse world of the Eocene, communities actually were little impacted by lithological changes associated with quantitatively-determined climatic perturbations. We demonstrate that the application of simple statistical measures can draw attention to unwarranted paleoecological ontological assumptions and avoid their being applied inappropriately to neoecological work.

Key Words: ontology; reproducibility; foraminifera; Ostracoda; Pleistocene; Paleocene-Eocene thermal maximum; assemblage turnover index; Milankovitch cycles; Ocean Drilling Program; Deep Sea Drilling Program

Introduction: The Nature of Ontology Confidence is paramount in science, which advances on a foundation of trusted discoveries. Reproducibility of the interpretation of the observations is vital if one scientist is to have confidence in another’s conclusions. However, oftentimes we need to question the assumptions that underlie the presented

1 Received on April 23, 2014. Accepted on April 25, 2014. Last revisions received on May 5, 2014. 2 Petroleum Geoscience Programme, Department of Chemical Engineering, University of the West Indies, St. Augustine, Trinidad and Tobago. E-mail: [email protected] 3 Smithsonian Institution, MRC-121, P O Box 37012, Washington DC 20013-7012 USA. E-mail: [email protected]

DOI:10.9784/LEB2(1)Wilson.01 Electronically available on May 16, 2014. Mailed on May 14, 2014. Life: The Excitement of Biology 2(1) 14

interpretation because they involve ontological decisions that are unrecognized. The adoption of quantitative techniques greatly aids in questioning those assumptions. Ontology is the branch of metaphysics that deals with the nature of being. The term "ontology" refers in philosophy to the manner in which an individual characterises observed phenomena (Libarkin and Kurdziel 2006). Sowa (2010) notes that ontology is a stable pattern of invariant signs that is fossilized in formal theories and does not develop further as each individual interacts with the world and other creatures in it. To adopt an ontological position is to adopt a perspective regarding the nature of the universe and to devise one’s interpretations from within that perspective. An ontological decision is made when a person makes an a prioi (before investigation) decision about the nature of the universe or some subset of it. For example, some communities believe that the Earth and universe were created together only a few thousand years ago, while others believe that the Earth formed over 4 billion years ago (Evans 2001). Those working in macro- sociology make the ontological assumption that society is either in balance and functions for the good of all (the functionalist perspective) or that it is rife with class conflict between those who buy and those who sell their labour (the Marxian conflict perspective) (Mooney et al. 2012). Once an ontological decision has been made, the person who has made it then proceeds to interpret the information regarding his/her surroundings, as provided by the senses, within the framework of that decision. All human beings organise their lives and interpretations around ontological assumptions. Some of these are scientifically warranted, as in the macro-sociologists’ adoption of contrary perspectives. Others, such as the belief in an Earth only a few thousand years old, are not supported by science. The belief in an ancient Earth is a somewhat flexible assumption as geologists have adjusted their understanding of the solar system’s age as evidence has accumulated. Here we are concerned with ontological assumptions that were adopted by paleoclimatic scientists but were not altered as evidence to the contrary was gathered.

Ontological decisions and the use of paleontological data for decision making in the recent and beyond In recent years paleoecology has become a powerful resource for ecologists and conservationists, the fossil record containing unique insights into how ecosystems function that cannot be determined by examining solely modern systems. The fossil record, for example, can provide a ‘deep time’ perspective on the response of communities to climate change. Here we consider results from impact studies of paleoclimatic change on biotic communities used as a basis for neoclimatic and ecological research and prediction, and show that results are not in accord with interpretations. First we consider the world during an icehouse state and examine glacial/interglacial Life: The Excitement of Biology 2(1) 15

transformations in the sedimentary, lithological and biotic fossil record as indicators of recent ecological changes with recent climate change. Then we examine as an exemplar the ontologically predicted relationship between climate, diversity and lithology in a greenhouse world, Lower Eocene section. Our objective is to instil a cautionary note for parallels with recent events into the uncritical use of paloecological results based upon inherent ontological assumptions

The impact of ontological decisions on the interpretation of the biotic impact of climate change during the Pleistocene Ever since Fourier (1824), Croll (1867, 1875) and Milankovitch (1930) recognized astronomically-forced climate fluctuations, there has been an ontological assumption that Pleistocene glacial–interglacial cycles greatly impacted global biota (e.g. Geikie 1874, Segota 1967, Fleming 2006), whether comprising terrestrial (e.g. Astorga and Pino 2011, Böcher 2012) or marine (e.g. Aguirre et al. 2011, Liu et al. 2011) organisms, including abyssal foraminifera (e.g. Schnitker 1974) and ostracodes (e.g. Alvarez Zarikian et al. 2009). Foraminifera are minute unicellular protists with fossilizable tests (Haynes 1981, Murray 2006) and ostracodes are microscopic, bivalved crustaceans (Horne et al. 2013), both of which are useful in assessing ancient (e.g. Smart 2003) and modern (e.g. Schönfeld et al. 2012) environmental and climate changes. Some authors have with apparent success sought to distinguish glacial and interglacial assemblages of foraminifera or ostracodes. Phleger et al. (1953) noted the presence in North Atlantic piston cores of ‘‘layers of [foraminiferal] faunas normal for their latitude alternating with faunas typical of a higher latitude.’’ Streeter (1973) found that Atlantic benthonic foraminifera at depths >2500 m varied greatly over the last 150 ka. He suggested that this arose because of depression and elevation of faunas through a depth range of several hundred meters between glacials and interglacials. However, paleontological research has not been completely successful in distinguishing glacial and interglacial assemblages (Roy et al., 1996). For example, although Streeter and Lavery (1982) recorded that uppermost Pleistocene foraminiferal faunas in cores from the western North Atlantic slope and rise were dominated by Uvigerina, but that Hoeglundina dominated in the Holocene, they further suggested that this faunal transition was diachronous, occurring at ~12 ka at 3,000 m, but at ~8 ka at 4,000 m. Thus, one cannot (a) characterise either assemblage as being definitely glacial or interglacial in origin and/or (b) use the change in the fauna to correlate the sedimentary successions at different paleodepths. Other studies, although they have made an ontological decision that there must have been glacial-interglacial regime shifts (i.e., fluctuations between steady ecological states that are not readily reversible (Genkai-Kato 2007)), have presented unconvincing evidence of distinct glacial and interglacial Life: The Excitement of Biology 2(1) 16

communities. Aksu et al. (1992) found glacial-interglacial, community-level regime shifts in coccoliths and dinoflagellates in the NE Labrador Sea but less persuasive evidence of regime shifts among planktonic foraminiferal assemblages, which were dominated by the polar-water indicator Neogloboquadrina pachyderma (Ehrenberg) with sinistral coiling. The authors wrote that N. pachyderma sinistral dominated most interglacial faunas before 0.5 Ma, which were therefore assumed to be ‘‘similar to those found in the glacial stages.’’ Didie and Bauch (2000) suggested that the ostracode fauna in the upper Pleistocene of Rockall Plateau, North Atlantic, fluctuated between a “mainly” interglacial Henryhowella-Pelecocythere-Echinocythereis-Cytherella- Bradleya-Aversovalva-Eucytherura assemblage and a glacial Acetabulastoma- Rhombobythere-Bythoceratina-Polycope-Pseudocythere assemblage that they wrote ‘‘appears’’ to be restricted to peak glacial periods. Hunt et al. (2005) made the ontological assumption that there should be glacial-interglacial contrasts in benthonic foraminiferal species richness (S) across glacial- interglacial cycles over the past 130 kyr in the deep-sea throughout the Atlantic and Pacific Oceans. However, they found statistically significant (p < 0.05) correlations between oxygen isotope-derived temperatures and S in only four of ten cores. Martinez et al. (2007) suggested that in western Caribbean Sea, Middle–Upper Quaternary planktonic foraminifera in the Sea, diversity measured using the information function H = –Σpi·ln(pi), where pi is the proportional abundance of the ith species] was during glacials depressed by the development of a deep thermocline. However, their data show that H did not differ between the interglacial marine isotope stage (MIS) 11 and MIS 12, and was lower during the interglacial MIS 13 than in the adjacent glacials MIS 12 and MIS 14. Some authors, seemingly having consciously avoided making an a priori assumption that there must have been distinct glacial and interglacial assemblages in all environments, have avoided stressing glacial-interglacial patterns and so found unexpected if subtle patterns (Roy et al., 1996). For example, Sen Gupta et al. (1982) examined Late Quaternary benthonic foraminifera in three cores taken near 2000 m from the eastern Caribbean Sea. They found that the assemblage changed only subtly at glacial-interglacial boundaries based on Globorotalia menardii (d’Orbigny, 1826) (for details, see Ericson and Wollin 1956, 1968; Martin et al. 1990). While not finding distinct glacial and interglacial communities, Sen Gupta et al. (1982) instead recorded some species-level contrasts, noting that Nuttallides umbonifera (Cushman, 1933), Bulimina buchiana Carpenter, Parker, and Jones, 1862 and Chilostomella oolina Schwager, 1878 were more common the last two glacials that in interglacials. Wilson (2012) used SHE analysis (Hayek and Buzas 1997) for the identification of abundance biozones (SHEBI – Buzas and Hayek 1998) when examining planktonic foraminiferal associations in three piston cores from the northeastern Caribbean Sea, and found that there was no relationship between Life: The Excitement of Biology 2(1) 17

abundance biozones and those glacial-interglacial boundaries based on Globorotalia menardii. The succession of abundance biozones differed between the three cores, although taken only ~150 km apart and from similar water depths, indicating that the region is one of considerable oceanographic complexity. This is reflected in the distinct benthonic foraminiferal associations found in these cores (Wilson 2011), which, once again, do not show any marked glacial-interglacial contrasts (Wilson 2008) but show that the organic flux in the northeast Caribbean Sea decreased gradually through the Late Quaternary. Wilson (2013) recorded a major regime shift during MIS 8–9 in the Upper Quaternary of ODP Hole 1006A (Santaren Channel, offshore western Bahamas), but otherwise found only weak evidence of Milankovich cycles, Globocassidulina subglobosa (Brady, 1881) and Cibicidoides aff. C. io (Cushman, 1931) being smaller assemblage components during some glacial MISs. However, the percentages of these species were not significantly correlated with one another. Wilson (2014), following an examination of benthonic foraminifera in the abyssal ODP Hole 994C (Blake Ridge, western Atlantic Ocean) using SHEBI, concluded that “community restructuring had no significant relationship to paleoclimatic events, including glacial cycles and terminations.” Hayek and Wilson (2013) developed a simple statistical measure, the assemblage turnover index (ATI), and showed that ATI in ODP Hole 994C peaked primarily during the transgressions associated with Pleistocene glacial terminations. They concluded that “the current inability to detect glacial- interglacial contrasts in general appears to arise because not all sites show marked changes in community composition at the species level at glacial- interglacial boundaries.” This is apparently because the onset of glacial conditions is a protracted process while deglaciation occurs rapidly (see Berger 2008, Figure 1). The slow onset induces only low levels of assemblage turnover in abyssal foraminiferal assemblages, while the rapid warming and influx of freshwater during deglaciation provoke a major and rapid restructuring of the community. In addition, Hayek and Wilson (2013, Table 3) showed that the species affected by the turnover differed between the peaks in ATI, such that one would not expect to find identical faunas in all glacials or all interglacials. This implies that glacial and interglacial conditions act as attractors comparable to a butterfly-shaped representation of the Lorenz attractor of Chaos Theory (Figure 1), in which minor differences in the initial conditions of any two or more systems (such as at, say, the onset of glacials or interglacials) prevent the perfect convergence of those systems onto a point representing a single state (Schaffer 1985, Holden and Muhamad 1986, Chang 2013). Thus, the details of the abyssal foraminiferal assemblage in one glacial cannot be predicted from those of the assemblage in the preceding glacial. This shows that the precise development of the modern assemblage cannot be modelled using the Pleistocene record, which can only be used to suggest general trends. Life: The Excitement of Biology 2(1) 18

Ontological decisions and interpretations of the impact of Early Eocene climate change Here we present a second example of the interface between paleoecology and ecology. This one is from the greenhouse world of the Early Eocene and is for comparative use with present day climate changes under the global warming documented to have occurred over recent past centuries. Recent years have seen increased interest in Early Eocene paleoclimates (Kaiho 1991, Katz and Miller 1991, Thomas 1992, Kaiho 1994, Thomas and Shackleton 1996, Lourens et al. 2005, Higgins and Schrag 2006, Miller et al. 2008, D'haenens et al. 2012, Galeotti et al. 2012). A major warming at the Palaeocene-Eocene boundary (the Paleocene–Eocene thermal maximum, PETM, about 55 myr) has been identified as being the single largest, well-documented warming event in the history of the Earth (Zachos et al. 2007). It was accompanied by a major carbon isotope excursion (CIE – Kennett and Stott 1991) and is thought to have had considerable biotic impacts (Sluijs et al. 2007).

Figure 1. The butterfly-shaped Lorenz attractor of Chaos Theory shown in the x/z plane.

It is, however, only the most extreme of a series of such events during the Late Palaeocene and Early Eocene (Thomas and Zachos 2000). Oxygen and carbon stable isotope records show quantitatively that during the PETM global Life: The Excitement of Biology 2(1) 19

temperature rose by >5–8°C in <10 kyr and remained high for some tens of thousands of years before gradually abating. Ocean acidification and carbonate dissolution during the PETM led to the deposition at bathyal and abyssal depths of condensed, clay rich Palaeocene–Eocene boundary sections (Thomas et al. 1999, Takeda and Kaiho 2007, Zachos et al. 2007). Similar clay-rich horizons of Early Eocene age have been ascribed to other hyperthermal events. Lourens et al. (2005) found a carbonate-poor, red clay (the Elmo horizon) in deep-sea cores from Walvis ridge, Antarctica, and estimated it to have been deposited ~ 2 million years after the PETM. The Elmo horizon being coincident with carbon isotope depletion events elsewhere, Lourens et al. (2005) suggested it to be a second global thermal maximum. It may thus be equivalent to the Eocene Thermal Maximum 2 (ETM2; ∼53.7 Ma) recorded by Stap et al. (2010) from Ocean Drilling Program Sites 1265, 1267, and 1263 (Walvis Ridge, SE Atlantic Ocean). Cramer et al. (2003) found numerous rapid (40–60 kyr duration) negative excursions of up to 1% in carbon isotope records for upper Paleocene– lower Eocene sections at widely separated (North Atlantic, Pacific and Southern Ocean) Ocean Drilling Program and Deep Sea Drilling Project Sites coincident with maxima in the Earth’s orbital eccentricity. This resulted in high-amplitude variations in insolation due to forcing by climatic precession. These they used to correlate the four sites, labelling them events A–L, with paired events being individually identified with a 1 or 2 after the letter. Lourens et al. (2005) concluded the Elmo horizon to be correlative with event H1 of Cramer et al. (2003). However, sedimentological evidence of all these events is not found everywhere. The Shipboard Scientific Party for Ocean Drilling Program (ODP) Leg 207, located on the Demerara Rise off Surinam, South America (Shipboard Scientific Party 2004), found a single clay rich horizon in ODP Hole 1259B that they ascribed to the PETM. However, their visual core descriptions for this and the accompanying Holes 1259A and 1259C do not show any other clay rich horizons that may be correlated with A–L of Cramer et al. (2003). D'haenens et al. (2012) found five marl (calcareous claystone) beds within an otherwise chalky early Eocene section at DSDP Site 401 (Bay of Biscay — NE Atlantic), and labelled these α though ε (oldest to youngest). These clay-enriched levels they found to correspond to negative δ13C and δ18O bulk-rock excursions indicative of injections of 12C-enriched greenhouse gasses and small rises in temperature. They did not, however, correlate these with any of events A–K of Cramer et al. (2003). Where sedimentological evidence is found, it has not always been noted to be reflected in the biota. Wing and Harrington (2001) examined pollen in a 900 m section of the terrestrial Fort Union and Willwood Formations in the Bighorn Basin (NE Wyoming) that spans the Upper Paleocene and Lower Eocene. They found that there were no last appearances of common taxa at the Paleocene/Eocene boundary, and concluded on this basis that the modest level Life: The Excitement of Biology 2(1) 20

of floral change coincident with the PETM contrasts with the marked coeval taxonomic turnover and ecological rearrangement of North American mammalian faunas. They suggested that the faunal change probably resulted from faunal migration across Arctic land bridges that became habitable during the PETM, but that climatically sensitive plants were unable to migrate across these bridges. Thus, primary cause of terrestrial biotic change across the Paleocene/Eocene boundary was in Wyoming the result of interactions between immigrant and native taxa, not climate change directly. They did not, however, examine in detail the changes in proportional abundances of common species across the Paleocene-Eocene boundary. The PETM has been identified as causing a major extinction among bathyal and abyssal foraminifera (30–50% of species; see Thomas 1992). Lourens et al. (2005) found that in the Elmo horizon benthonic foraminiferal species richness is low and assemblages are dominated by diminutive Nuttallides truempyi and Abyssamina spp. This contrasts with Wilson’s (2014) finding that in the Upper Quaternary of ODP Hole 994C, benthonic foraminiferal diversity measured using the information function H was negatively correlated with palaeotemperature estimated from oxygen isotope ratios. This suggests that diversity may be depressed by stresses due to both hypothermal and hyperthermal events. Thus, those working on neoecology cannot yet make conclusive predictive statements concerning biotic change that will result solely from regarding impending events.

Using the assemblage turnover index (ATI) to sidestep ontology To avoid the impact of ontological decisions on interpretations of the impact of palaeoclimate change on biotic assemblages, Hayek and Wilson (2013) introduced two statistical indices to assess assemblage turnover, the assemblage turnover index (ATI) and the Conditioned on Boundary Index (CoBI) (See Appendix 1). Their use makes the statistical analyses of vectors of proportional data objective. They are here applied to an exemplar of foraminifera, but can be applied to any variable for which a series of proportional data over time are available (e.g. oxygen isotopes in an ice core, carbon isotopes in a sedimentary rock succession). D'haenens et al. (2012) made the ontological assumption that there must be changes in the foraminiferal fauna associated with the five Early Eocene marl beds in the chalky section at DSDP Site 401. They concluded that the foraminiferal record shows increased relative abundances of oligotrophic taxa (e.g. Nuttallides umbonifera) and a reduction in the abundance of buliminid species followed by an increase of opportunistic taxa (e.g. Globocassidulina subglobosa and Gyroidinoides spp.) coeval with several (but not all) of these lithological, presumably hyperthermal events. ATI shows that some marl levels (LATI-2 and LATI-4) coincided with low values of ATIs, but this was not true of all; ATIs was low at the base of LATI-6 but was higher within it, while LATI- Life: The Excitement of Biology 2(1) 21

8 entrained several peaks at which ATI s  x  . Thus, peaks in otherwise low background turnover as shown by ATIs do not coincide with changes in lithology and the marl levels do not all show either the same values or patterns of ATIs (Figure 2).

Figure 2. The between sample assemblage turnover index (ATIs) for benthonic foraminifera in the Lower Eocene at DSDP Site 401 (Bay of Biscay — NE Atlantic), data from D'haenens et al. (2012). Red indicates marl beds α – ε, green indicates odd- numbered peak bounded assemblage turnover intervals (PATIs). Dashed vertical line marks mean ATIs. Life: The Excitement of Biology 2(1) 22

Figure 3. The percentage abundance of Anomalinoides alazanensis in the Lower Eocene at DSDP Site 401 (Bay of Biscay — NE Atlantic). Data from D'haenens et al. (2012). Red bars at left indicate marl beds α – ε, green bars at right indicate odd-numbered peak bounded assemblage turnover intervals (PATIs).

The values for CoBIt are given in Table 1. No species contributed >0.02 (i.e., >2%) to CoBIt across all PATI or LATI boundaries. Only six species Life: The Excitement of Biology 2(1) 23

(Bolivina crenulata Loetterle, 1937, Bulimina virginiana Cushman, 1944, Cibicidoides eocaenus (Guembel, 1868), Globocassidulina subglobosa, Nuttallides umbonifera (Cushman, 1933), Pseudoparrella minuta Olsson, 1960) contributed >0.1 to CoBIt across one or more PATI or LATI boundaries. Anomalinoides alazanensis (Nuttall, 1932) contributed >0.02 to eight of ten LATI boundaries, but to only one of seven PATI boundaries. This suggests that the proportional abundances of A. alazanensis, rather than N. umbonifera, buliminids, G. subglobosa and Gyroidinoides spp. can be used to distinguish marly from chalky LATIs. However, closer examination shows that A. alazanensis is also of limited use in distinguishing hyperthermal from non- hyperthermal communities; while a graph of the proportional abundance of A. alazanensis through D'haenens et al.’s (2012) section (Figure 3) shows that it was rarer in the marly LATIs 2 and 4 than in the bounding chalky LATIs 1, 3 and 5, also shows that it was as abundant in the marly LATI-6 as in the chalky LATI-7. There is, therefore, no constancy in foraminiferal assemblages in the marly horizons and any ontological decision that the factors governing the development of the marls, whether palaeoclimatic or otherwise, also impacted on the foraminifera to produce identical assemblages, is unwarranted.

Conclusion: Beyond Ontology There is in science no theory-neutral interpretation. No matter what phenomenon we observe, we interpret it in terms of our previous experience. This can lead to making unwarranted ontological decisions, as was the case of glacial-interglacial contrasts envisaged by Aksu et al. (1992) , Didie and Bauch (2000), Hunt et al. (2005) and Martinez et al. (2007) and the changes in fauna between Eocene chalks and marls envisaged by D'haenens et al. (2012). This is especially misleading when either (a) an author conducts a quantitative and objective statistical analysis but interprets the results subjectively or selectively such as we showed with studies using statistical methods on Pleistocene data or (b) sees a change in one factor (e.g. palaeoclimate, lithology) and assumes that it must be reflected in another factor (e.g. faunal assemblage) as we showed in Eocene examples.Those undertaking analyses must be aware of their ontological decisions and must beware of letting them guide their interpretations. Those who seek to apply paleoecological results to neoecological work cannot as yet make conclusive or predictive statements based only upon the hypothesized similarity of biotic, lithologic or climactic past scenarios. The adoption of statistical methodology is not sufficient to provide evidence of unwarranted assumptions without knowledge of the underlying probabilistic structure while the use of objective analytical approaches such as ATI and CoBI can draw attention to many ontological decisions that authors may have adopted.

Life: The Excitement of Biology 2(1) 24

LATI-10\11

0.02

0.08

0.02

0.04

0.16

0.03

0.19

0.03

0.02

0.05

0.03

0.02 ores ores

LATI-9\10

0.03

0.02

0.03

0.07

0.03

0.25

0.02

0.06

0.03

0.11

0.03

0.02

0.07 0.04

LATI-8\9

0.03

0.02

0.08

0.02

0.17

0.06

0.02

0.03

0.14

0.02

0.03

0.02

0.05

0.03

0.05

0.03 t

LATI-7\8

0.04

0.02

0.03

0.14

0.03

0.06

0.03

0.05

0.12

0.05

0.04

0.05

0.07

0.04

0.03 0.04

LATI-6\7

0.03

0.02

0.03

0.09

0.02

0.05

0.03

0.04

0.03

0.12

0.04

0.05

0.03

0.08

0.02 0.04

LATI-5\6

(2012). Bold indicates sc

0.04

0.03

0.08

0.05

0.03

0.04

0.03

0.02

0.09

0.04

0.02

0.03

0.04

0.00

0.12

0.02

0.05

0.06 0.02

LATI-4\5

0.03

0.02

0.12

0.08

0.21

0.03

0.06

0.08

0.04

0.09

0.02

LithologybasedCoBI

LATI-3\4

0.03

0.02

0.14

0.05

0.26

0.02

0.06

0.03

0.05

0.03

0.02

0.05 0.03

LATI-2\3

0.02

0.03

0.08

0.03

0.02

0.07

0.02

0.06

0.05

0.07

0.06

0.05

0.10

0.03 0.04

LATI-1\2

0.02

0.03

0.02

0.08

0.05

0.03

0.08

0.06

0.20

0.02

0.03

0.09 0.04

PATI-7\8

0.04

0.03

0.04

0.11

0.03

0.13

0.04

0.07

0.03

0.19

0.03

0.05 0.04

PATI-6\7

0.04

0.02

0.12

0.03

0.04

0.11

0.03

0.04

0.03

0.09

0.05

0.07

0.08

0.05

0.02

PATI-5\6

0.03

0.09

0.03

0.20

0.02

0.04

0.14

0.02

0.04

0.03

0.04

0.03

0.06

NE NE Atlantic). Data from D'haenens et al.

PATI-4\5

—

0.07

0.03

0.09

0.04

0.15

0.03

0.04

0.05

0.11

0.05

0.05 0.04

PATI-3\4

ClassicalCoBI

0.04

0.07

0.03

0.05

0.03

0.05

0.03

0.12

0.07

0.06

0.05

0.03

0.06

0.03

0.03 0.02

PATI-2\3

0.05

0.04

0.13

0.14

0.02

0.04

0.02

0.09

0.03

0.04

0.02

0.03 0.04

PATI-1\2

0.03

0.02

0.06

0.16

0.12

0.03

0.05

0.06

0.12

0.07

sp.

Table 1. Classical Thorough Conditioned Foraminifera from DSDP on Site 401 (Bay of Biscay Boundary Index (CoBIt) and of 0.10. > CoBIt Lithological based CoBIt for Lower Eocene

Tappaninaselmensis

Turrilinabrevispira

Siphoninatenuicarinata

Stilostomellaplummerae

Seabrookialagenoides

Stilostomellagracillima

Rosalina

Praebulimina

Praebuliminareussi

Pleurostomellapaleocenica

Pseudoparrellaminuta

Oridorsalisumbonatus

Osangulariamexicana

Nutallidesumbonifera

Nuttalidestruempyi

Nonionhavanense

Heronalleniapusilla

Globocassidulinasubglobosa

Gyroidinanaranjoensis

Gyroidinoidescomplanata

Benthonicforaminifera indet.

Eponidesbollii

Discorbis

Dentalina

Coryphostoma

Cibicidoidesungerianus

Cibicidoideseocaenus

Buliminavirginiana

Buliminatuxpamensis

Buliminathanetensis

Buliminellasemicostata

Buliminellagrata

Bolivinacrenulata

Brizalinacarinata

Anomalinoidespraespissiformis

Angulogerinamuralis

Aragoniaaragonensis

Anomalinoidesalazanensis Species Life: The Excitement of Biology 2(1) 25

LATI-10\11

- -

------

0.02

0.08

0.02

0.04

0.16

0.03

0.19

0.03

0.02

0.05

0.03 0.02 0.02 0.03 0.05 0.02 0.03 0.03 0.19 0.03 0.03 0.03 0.16 0.04 0.02 0.08 0.02 0.02

LATI-9\10

- -

------

0.03

0.02

0.03

0.07

0.03

0.25

0.02

0.06

0.03

0.11

0.03

0.02

0.07 0.04 0.04 0.07 0.02 0.02 0.03 0.11 0.03 0.06 0.02 0.25 0.03 0.03 0.07 0.03 0.02 0.03

LATI-8\9

- -

------

0.03

0.02

0.08

0.02

0.17

0.06

0.02

0.03

0.14

0.02

0.03

0.02

0.05

0.03

0.05 0.03

0.03 0.05 0.03 0.05 0.02 0.03 0.02 0.14 0.03 0.02 0.06 0.17 0.02 0.08 0.02 0.02 0.03

t t

LATI-7\8

- -

------

0.04

0.02

0.03

0.14

0.03

0.06

0.03

0.05

0.12

0.05

0.04

0.05

0.07

0.04

0.03 0.04 0.04 0.03 0.04 0.07 0.05 0.04 0.05 0.12 0.05 0.03 0.06 0.03 0.14 0.03 0.03 0.02 0.04

LATI-6\7

- -

------

0.03

0.02

0.03

0.09

0.02

0.05

0.03

0.04

0.03

0.12

0.04

0.05

0.03

0.08

0.02 0.04 0.04 0.02 0.08 0.03 0.03 0.05 0.04 0.12 0.03 0.04 0.04 0.03 0.05 0.02 0.09 0.03 0.02 0.03

LATI-5\6

- -

------

0.04

0.03

0.08

0.05

0.03

0.04

0.03

0.02

0.09

0.04

0.02

0.03

0.04

0.00

0.12

0.02

0.05

0.06 0.02 0.02 0.06 0.05 0.02 0.12 0.00 0.04 0.03 0.02 0.04 0.09 0.02 0.03 0.03 0.04 0.03 0.05 0.08 0.03 0.04

LATI-4\5

- -

------

0.03

0.02

0.12

0.08

0.21

0.03

0.06

0.08

0.04

0.09 0.02

0.02 0.09 0.04 0.08 0.06 0.03 0.21 0.08 0.12 0.02 0.03

LithologybasedCoBI LithologybasedCoBI

LATI-3\4

- -

------

0.03

0.02

0.14

0.05

0.26

0.02

0.06

0.03

0.05

0.03

0.02

0.05 0.03 0.03 0.05 0.02 0.03 0.05 0.03 0.06 0.02 0.02 0.26 0.05 0.14 0.02 0.03

LATI-2\3

- -

------

0.02

0.03

0.08

0.03

0.02

0.07

0.02

0.06

0.05

0.07

0.06

0.05

0.10

0.03 0.04 0.04 0.03 0.10 0.05 0.06 0.07 0.05 0.06 0.06 0.02 0.07 0.02 0.03 0.08 0.03 0.02

LATI-1\2

- -

------

0.02

0.03

0.02

0.08

0.05

0.03

0.08

0.06

0.20

0.02

0.03

0.09 0.04 0.04 0.09 0.03 0.03 0.02 0.20 0.06 0.08 0.03 0.05 0.08 0.02 0.03 0.02

PATI-7\8

- -

------

0.04

0.03

0.04

0.11

0.03

0.13

0.04

0.07

0.03

0.19

0.03

0.05 0.04 0.04 0.05 0.03 0.19 0.03 0.07 0.04 0.13 0.03 0.11 0.04 0.03 0.04

PATI-6\7

- -

------

0.04

0.02

0.12

0.03

0.04

0.11

0.03

0.04

0.03

0.09

0.05

0.07

0.08

0.05 0.02

0.02 0.05 0.08 0.07 0.05 0.09 0.03 0.04 0.03 0.11 0.04 0.03 0.12 0.02 0.02 0.04 0.04

t t PATI-5\6

PATI-5\6

- -

------

0.03

0.09

0.03

0.20

0.02

0.04

0.14

0.02

0.04

0.03

0.04

0.03 0.06 0.06 0.03 0.04 0.03 0.04 0.02 0.14 0.04 0.02 0.20 0.03 0.03 0.09 0.03 0.03

PATI-4\5

- -

------

0.07

0.03

0.09

0.04

0.15

0.03

0.04

0.05

0.11

0.05

0.05 0.04 0.04 0.05 0.05 0.05 0.11 0.05 0.04 0.03 0.15 0.04 0.09 0.03 0.07

PATI-3\4

- -

------

ClassicalCoBI

0.04

0.07

0.03

0.05

0.03

0.05

0.03

0.12

0.07

0.06

0.05

0.03

0.06

0.03

0.03 0.02 0.02 0.03 0.03 0.06 0.03 0.05 0.06 0.07 0.12 0.03 0.05 0.03 0.05 0.03 0.07 0.04

PATI-2\3

- -

------

0.05

0.04

0.13

0.14

0.02

0.04

0.02

0.09

0.03

0.04

0.02

0.03 0.04 0.04 0.03 0.02 0.04 0.04 0.03 0.03 0.09 0.02 0.02 0.04 0.04 0.02 0.14 0.13 0.04 0.05

PATI-1\2

- -

------

0.03

0.02

0.06

0.16

0.12

0.03

0.05

0.06

0.12 0.07

0.07 0.12 0.06 0.05 0.03 0.12 0.16 0.06 0.06 0.02 0.02 0.03 sp.

sp. sp.

sp.

Tappaninaselmensis

Turrilinabrevispira

Siphoninatenuicarinata

Stilostomellaplummerae

Seabrookialagenoides

Stilostomellagracillima

Rosalina

Praebulimina

Praebuliminareussi

Pleurostomellapaleocenica

Pseudoparrellaminuta

Oridorsalisumbonatus

Osangulariamexicana

Nutallidesumbonifera

Nuttalidestruempyi

Nonionhavanense

Heronalleniapusilla

Globocassidulinasubglobosa

Gyroidinanaranjoensis

Gyroidinoidescomplanata

Benthonicforaminifera indet.

Eponidesbollii

Discorbis

Dentalina

Coryphostoma

Cibicidoidesungerianus

Cibicidoideseocaenus

Buliminavirginiana

Buliminatuxpamensis

Buliminathanetensis

Buliminellasemicostata

Buliminellagrata

Bolivinacrenulata

Brizalinacarinata

Anomalinoidespraespissiformis

Angulogerinamuralis

Aragoniaaragonensis

Anomalinoidesalazanensis Species Species Anomalinoidesalazanensis Aragoniaaragonensis Angulogerinamuralis Anomalinoidespraespissiformis Brizalinacarinata Bolivinacrenulata Buliminellagrata Buliminellasemicostata Buliminathanetensis Buliminatuxpamensis Buliminavirginiana Cibicidoideseocaenus Cibicidoidesungerianus Coryphostoma Dentalina Discorbis Eponidesbollii Benthonicforaminifera indet. Gyroidinoidescomplanata Gyroidinanaranjoensis Globocassidulinasubglobosa Heronalleniapusilla Nonionhavanense Nuttalidestruempyi Nutallidesumbonifera Osangulariamexicana Oridorsalisumbonatus Pseudoparrellaminuta Pleurostomellapaleocenica Praebuliminareussi Praebulimina Rosalina Stilostomellagracillima Seabrookialagenoides Stilostomellaplummerae Siphoninatenuicarinata Turrilinabrevispira Tappaninaselmensis Life: The Excitement of Biology 2(1) 26

Acknowledgements Author BW would like to express his thanks to Stuart Toddington, who originally introduced him to ontology.

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Appendix 1 Hayek and Wilson (2013) presented two types of analysis. The first, in which species’ proportional abundances alone are considered, is here termed Classical Analysis of ATI. The second, in which both species’ proportional abundances and lithology are considered, is here termed Lithological Analysis of ATI. In Classical Analysis of ATI, the ATI is initially calculated for each pair of adjacent samples in a time series. It is defined as

Life: The Excitement of Biology 2(1) 30

ATI   pi2  pi1 (1), in which pi1 and pi2 are the proportional abundances of the ith species, i = 1,…, s, in the lower and upper samples. The summation sign was inadvertently omitted in the original publication of Hayek and Wilson (2013).). This assemblage turnover index between samples is denoted as ATIs. The mean x and standard deviation σ are calculated for the series of ATIs and for Classical Analysis of ATI are used to determine control charts and values for which

ATIs  x   . These peaks in ATIs indicate the positions of relative major assemblage turnovers (Hayek and Wilson, 2013), and are used to divide the succession into peak-bounded ATIs (PATI-) intervals. These intervals were numbered, commencing from PATI-1 for the oldest. PATI-1 and the uppermost PATI are of necessity incomplete, their lower and upper boundaries respectively not being bounded by peaks in ATIs. In Lithological Analysis of ATI, for comparison, the succession is divided into intervals defined by lithology, here termed LATI intervals, which are numbered, commencing from LATI-1 for the oldest. The positions of the peaks in ATIs (i.e., the PATI boundaries) are compared with the LATI boundaries. Hayek and Wilson (2013) presented also a thorough conditioned-on- boundary index CoBIt that assesses which species contributed most to the ATI at PATI and LATI boundaries. That is, CoBIt presents the proportion that each species within an assemblage contributed to the turnover across the PATI or LATI boundary. For each species at any boundary

CoBI  pi2  pi1 / ATI (2), where pij, j=1,2 are the ith species proportions in the PATIs or LATIs on either side of the selected boundary of interest and at which the ATI is calculated. In CoBIt, then, the ATI is denoted as ATIt and is calculated between the values in two complete PATIs or LATIs. The value of ATIt is substituted into equation (2), as are pi1 and pi2, the proportional abundance of the ith species in intervals (PATIs or LATIs) being compared. The proportional contribution of each species to the value of ATIt is assessed from the vector of thorough CoBI for each PATI or LATI boundary.

Life: The Excitement of Biology 2(1) 31

The morphology and histology of the male reproductive system in Apodiphus amygdali (Germar, 1817) (Hemiptera: Heteroptera: Pentatomidae)4

Nurcan Özyurt5, Selami Candan2, and Zekiye Suludere2

Abstract: This paper reveals the morphology and histology of the adult male reproductive system in the stink bug, Apodiphus amygdali (Germar, 1817), using light and scanning electron microscopy. Males have a pair of testes situated laterally to the alimentary canal, a pair of elongated cylindrical vasa deferentia and seminal vesicles, which join in a complex bulbus ejaculatorius, a ductus ejaculatorius, a pair of ectodermal sacs, a pair of accessory glands, and the phallus. Each testis consists of seven testicular follicles connected to the vas deferens. Each follicle contains a germarium, followed apically by growth zones where spermatozoa differentiate in the direction of the vasa deferentia. Each testis is connected to the seminal vesicle by a vas deferens. The seminal vesicles are connected to the bulbus ejaculatorius, which is surrounded by the tubularly coiled accessory glands. The bulbus ejaculatorius is continuous with the ductus ejaculatorius and connects to the aedeagus demonstrating its ectodermic origin.

Key Words: Spermatogonia, spermatocytes, spermatids, spermatozoa, light and scanning electron microscope (SEM)

Most insect species in the Heteroptera (Insecta: Hemiptera), including those in the family Pentatomidae, are phytophagous. Pentatomids are called stink bugs or shield bugs. Many of them are considered agricultural pests, because they can create large populations that feed on crops damaging production. Many heteropterans are a threat to cotton, corn, sorghum, soybeans, as well as many native and ornamental trees, shrubs, vines, weeds, and cultivated crops worldwide (Schuh and Slater, 1995; Schaefer and Panizzi 2000). There are very few studies of the morphology and histology of the reproductive system in pentatomids (Pendergrast, 1956; Ramamurty 1969; Adams 2001; Özyurt et al., 2013a, 2013b). Apodiphus amygdali (Germar, 1817) (Pentatominae: Haliini) is known as the Large Tree Pentatomid (Lodos, 1986; Bolu et al., 2006; Candan and Suludere, 2010, also see photo on page 41 this issue). Apodiphus amygdali, which is also known as the Fruit Trees Stink Bug, is distributed in Europe and the Middle East. Among the trees attacked by A. amygdali there are fruit trees, such as plum (Prunus domestica L., Rosaceae),

4 Received on September 5, 2013. Accepted on March 11, 2014. Last revisions received on April 8, 2014. Although this paper was received on September 5, 2013, email malfunction caused the Editor-in-Chief (JASB) to became aware that the authors intended to submit the paper on February 15, 2014. Once the misunderstanding was clarified, the paper was processed expeditiously. 5 Gazi University, Faculty of Science, Department of Biology, 06500 Teknikokullar, Ankara, Turkey. Emails: [email protected] (NÖ), [email protected] (SC), [email protected] (ZS).

DOI:10.9784/LEB2(1)Ozyurt.01 Electronically available on May 16, 2014. Mailed on May 14, 2014. Life: The Excitement of Biology 2(1) 32

apricot (Prunus armeniaca L., Rosaceae), apple (Malus pumila Mill., Rosaceae), olive (Olea europaea L., Oleaceae), pear (Pyrus communis L., Rosaceae) and pistachio (Pistacia vera L., Anacardiaceae) as well as non-fruit trees, like poplar (Populus alba L., Salicaceae), Turkish pine (Pinus brutia Ten., Pinaceae), plane- tree (Platanus orientalis L., Platanaceae), alma (Ulmus minor Mill., Ulmaceae), and willow bark (Salix alba L.,, Salicaceae) (Muhammed and Al-Iraqi, 2010). Considering the economic importance of A. amygdali, this study describes the morphology and histology of its reproductive system. Some of the findings contribute new characters for systematic studies of this group. The male reproductive system of Heteroptera presents five distinct regions (Figure 1): a pair of testes (t), two vas deferentia (t), two seminal vesicles (vs), an ectodermal sac (es), a bulbus ejaculatorius (b), a ductus ejaculatorius (d), and an aedeagus (not shown) (Pendergrast, 1956; Nijhout, 1994; Chapman 1998; Karakaya et al., 2012; Özyurt et al., 2013a, 2013b).

Figure 1. Male reproductive organs, t - testis, v - vas deferens, vs - vesicula seminalis, es - sac of ectodermal origin, eg - ectadene accessory gland, mg- mesadene accessory gland, b - bulbus ejaculatorius, d - ductus ejaculatorius (Pendergrast, 1956). Scale bar = 1 mm. The image has been reproduced, with small modifications, with permission of Royal Society of New Zealand.

Life: The Excitement of Biology 2(1) 33

The testes (Figure 1, t) consist of a great number of tubules that enter the vasa deferentia. The vasa deferentia (v) extend from the testes to paired seminal vesicles (vs). These vesicles insert on the anterior medial portion of the bulbus ejaculatorius (b). The bulbus ejaculatorius is covered by irregularly shaped accessory glands (eg and mg). The accessory glands of male insects can be classified into two types according to their mesodermal (mg) or ectodermal (eg) derivation. Almost all accessory glands that have been studied are of mesodermal origin, while little is known about those that have an ectodermal origin. Secretions of the male accessory glands from the spermatophore contribute to the seminal fluid that nourishes the spermatozoa during transport to the female. These secretions are also involved in the activation of spermatozoa and may alter female behavior (Pendergrast, 1956; Davey and Krieger, 1985; Chapman, 1998). The bulbus ejaculatorius is continuous with that of the ductus ejaculatorius (d). In most insects, there is a single ductus ejaculatorius, located medially and bearing a cuticular cover, demonstrating is ectodermic origin (Pendergrast, 1956; Davey and Krieger, 1985; Chapman, 1998; Karakaya et al., 2012; Özyurt et al. 2013a; Özyurt et al. 2013b).

Methods Gross Anatomy. Adult males A. amygdali were collected in July 2011 in Antalya, Turkey. The specimens were killed with ethyl acetate and dissected in 70% ethyl alcohol under a stereomicroscope. For the morphological studies, the dorsal cuticle was first removed from the prothorax to the last full-sized abdominal segments. Subsequently, the epidermis and the digestive system were removed. Two insect pins were inserted laterally through the last full-sized sternite to spread apart the abdomen and to expose the base of the reproductive system attached to the genital segments. The gross morphology of the reproductive systems of the males were examined and photographed with a Leica EZ4D stereomicroscope. Light Microscopy. For the histological analysis, the reproductive systems of ten males were fixed in Bouin’s for 24h. Thereafter, the tissues were washed, dehydrated in a series of ethanol solutions (70%, 80%, 90%, 100%) and finally embedded in paraffin. Paraffin sections were cut into 6-7 µm slices and stained with Hematoxylin-Eosin and Mallory’s triple stain for light microscopic examination (Junqueira and Junqueira, 1983). The sections were viewed and photographed by using an Olympus BX51 compound microscope. Scanning Electron Microscopy (SEM). Cleaned and dried (Polaron CPD 7501 Critical Point Dryer) specimens were mounted using double sided sticky tape on SEM stubs, coated with gold in a Polaron SC 502 sputter coater, and examined with a scanning electron microscope (JEOL JSM 6060 LV) at 5kV.

Life: The Excitement of Biology 2(1) 34

Results The internal male reproductive system of A. amygdali is formed by a pair of testes, a pair of vas deferentia, a pair of seminal vesicles, a pair of accessory glands, a bulbus ejaculatorius, a ductus ejaculatorius and aedeagus (Figure 2a). The testes are paired, cylindrical and red (testes are already noticed in freshly in emerged adults) (Figure 2a) lie at the sides of the alimentary tract, approximately in the middle of the abdominal cavity. The testis is composed by seven sperm tubes surrounded by tunica propria, peritoneal sheath with embedded tracheoles (Figures 2a, 2b). Sperm develops in the testes and is stored in the seminal vesicles (Figure 2b) until the mating occurs.

Figure 2. a. Light micrograph of general morphology of the male reproductive system in Apodiphus amygdali. Testes (T), vas deferens (Vd), seminal vesicle (Vs), bulbus ejaculatorius (B), ductus ejaculatorius (D), accessory glands (Ag), aedeagus (A). Scale bar = 2 mm. b. Longitudinal section of the testes surrounded by peritoneal sheath (Ps) with embedded tracheoles (Tr) and showing the follicles (F). Growth zone (Gz), maturation zone (Mz), differentiation zone (Dz), vas deferens (Vd), seminal vesicles (Vs). Scale bar = 500 µm.

Spermatogenesis occurs within the lumen of the sperm tubes; different stages of spermatogenesis can be observed across the sperm tubes. Spermatogenesis begins in the germarium, where spermatogonia develop and proliferate within cysts. As both mitotic and meiotic divisions take place, the cysts that contained the spermatogonia degenerate. Spermatogonia differentiate Life: The Excitement of Biology 2(1) 35

into spermatocytes before becoming spermatids (Figures 3 a-f). The spermatids differentiate into spermatozoa as they approach the vas deferens.

Figure 3. a-b. The presence of the spermatocytes (Sp) forming cysts (Cy) in growth zone of the testes follicles and sperm tubes surrounded by tunica propria Light and scanning electron microscopy (respectively). c-d. Light and SEM photos of the presence of spermatocytes at different developmental stages and differentiated spermatids (St). e-f. Light and SEM photos of the presence of spermatids in maturation zone of the testes follicles. Bar on a, c, and e = 100 µm; on b and d = 20 µm; on f = 10 µm. Life: The Excitement of Biology 2(1) 36

Figures 4. a-b. Light and SEM photos of spermatozoa (Sz) bundles in differentiation zones the testes follicles. c-d. Longitudinal (c) and cross sections (d) of seminal vesicles (Vs) and vas deferens (Vd) with large numbers of spermatozoa bundles, epithelium (Ep) and muscle sheath (Ms). e-f. SEM photos of large numbers of spermatozoa bundles in epithelium sheath. Bar on c, c, and d = 100 µm; on b and d = 10 mm; on e = 20 mm.

The spermatozoa are contained in cysts which are grouped together in bundles and from which the spermatozoa are liberated (Figures 4 a, b). The vas deferens is the duct leading from the testes to the seminal vesicle. Within this simple tube spermatozoa are being transported to the seminal vesicles. A portion of each vas deferens and seminal vesicle is dilated to form a tubular chamber. The heads of the spermatozoa are embedded in the epithelial lining of the seminal vesicles and their tails extend posteriorly in a spiral into lumen. There is no outstanding difference between the histology of the vas deferens and the seminal vesicle. The walls of these ducts consist of an inner layer of epithelial cells which is surrounded by a network of muscle fibers extending in various Life: The Excitement of Biology 2(1) 37

directions. Epithelial cells of the ducts are cuboidal and they contain large spherical and well stainable nuclei (Figures 4c- f).

Figures 5. a-b. SEM and light photos showing of bulbus ejaculatorius (B), ductus ejaculatorius (D) and accessory glands (Ag) in male reproductive system. c-d. Light photos showing of muscle sheath (Ms) and epitelium (Ep) in bulbus ejaculatorius. e-f. SEM and light photo showing of accessory glands. Scale bar on a = 1 mm; on b-d, f = 100 µm; on e = 500 µm.

Life: The Excitement of Biology 2(1) 38

The seminal vesicle connects the bulbus ejaculatorius which is balloon shaped (Figure 5a). It is partly covered by an epithelium, here termed the investing epithelium. The walls of bulbus ejaculatorius are formed by muscles running concentric to the lumen of the ducts (Figures 5c, d). The ductus ejaculatorius has an inner and outer epithelium, with a band of striated muscle between them. The striated muscle consists of muscle cells that presumably contract in waves to generate a peristaltic movement. This would facilitate the movement of the sperm along the ductus ejaculatorius (Figure 5b). The bulbus ejaculatorius and the ductus ejaculatorius are covered by irregularly shaped accessory glands, which have multi-lobed tubular structures and an abundant supply of tracheae (Figures 5e, f).

Discussion Studies on the testicular ultrastructure and spermatogenesis must be encouraged to broaden our knowledge of the morphology and histology of the male reproductive system in insects. While in some Pentatomidae the general morphological and histological patterns are similar (Davis, 1956; Pendergrast, 1956; Lemos et al., 2005; Jahnke et al., 2006; Papáček and Soldán, 2008; Rodrigues et al., 2008; Wieczorek and Swiatek, 2009; Freitas et al., 2010; Karakaya et al., 2012; Özyurt et al., 2013a; Özyurt et al., 2013b), the results of this study support the existence of differences with regards location, size, shape and color of A. amygdali male reproductive system when compared to other Heteroptera. Every testis contain the testicular follicles where are produced spermatozoa. The number of follicles varies widely between species and has taxonomic importance (Davis, 1956; Pendergrast, 1956; Lemos et al., 2005; Jahnke et al., 2006; Papáček and Soldán, 2008; Rodrigues et al., 2008; Wieczorek and Swiatek, 2009; Freitas et al., 2010; Karakaya et al., 2012; Özyurt et al., 2013a; Özyurt et al., 2013b). Testes in A.amygdali and Perillus bioculatus (Fabricius) (Pentatomidae: Asopinae) (Adams, 2001) consists of seven sperm tubes, but in Nezara viridula (Linnaeus), Podisus nigrispinus (Dallas), Dolycoris baccarum (Linnaeus), Graphosoma lineatum (Linnaeus) (Pentatomidae), and Aphelocheirus aestivalis Fabricius (Heteroptera: Aphelocheiridae) 4-6 sperm tubes are observed (Lemos et al., 2005; Ramamurty, 1969; Özyurt et al., 2013a; Özyurt et al., 2013b). In Adparaproba gabrieli Carvalho (Heteroptera: Miridae), two follicles are observed (Uceli et al., 2011). The sperm tubes of A. amygdali as in other heteropterans are covered by a peritoneal sheath and a tunica propria (Davis, 1956; Chapman, 1998; Pires et al., 2007; Rodrigues et al., 2008; Karakaya et al., 2012; Özyurt et al., 2013a; Özyurt et al., 2013b). The testes contain sperm cells at different stages of spermatogenesis across the sperm tubes. The mechanisms of spermatogenesis in A.amygdali, including sperm differentiation, are rather similar in other Heteroptera (Bowen, 1922; Davis, 1956; Engelmann, 1970; Chapman, 1998; Lemos et al., 2005; Pires et al., Life: The Excitement of Biology 2(1) 39

2007; Rodrigues et al., 2008; Karakaya et al., 2012; Özyurt et al., 2013a; Özyurt et al., 2013b). Once fully developed, the sperm cells travel from the testes to the seminal vesicle via the vas deferens. However, in Notonecta glauca (Linnaeus, 1758) (Heteroptera: Notonectidae), the testicular follicles are directly connected to the seminal ducts (vasa deferentia laterals) (Papáček, and Soldán, 2008). In A.amygdali, as in other heteropterans, a portion of each vas deferens and seminal vesicle is dilated to form a tubular chamber. The walls of these ducts consist of an inner layer of epithelial cells that is surrounded by network of muscle fibers extending in various directions. Similar ductal structures have been observed in vasa deferentia and seminal vesicles of D. baccarum, G. lineatum, N. glauca (Papáček and Soldán, 2008; Özyurt et al., 2013a; Özyurt et al., 2013b). As within other Heteroptera, the seminal vesicles of A. amygdali connect to balloon-shaped bulbus ejaculatorius and are covered by irregularly shaped accessory glands (Özyurt et al., 2013a; Özyurt et al., 2013b). The bulbus ejaculatorius join to form a common ductus ejaculatorius (Bushrow et al., 2006). The terminal portion of the ductus ejaculatorius may be sclerotized to form the intromittent organ, the aedeagus. It differentiates from a pair of ectodermal lobes associated with the ninth abdominal segment and is often concealed within a genital chamber (Klowden, 2007). The morphological knowledge of insect male reproductive accessory glands of insects is extensive (Papáček, and Soldán, 2008). These structures vary considerably in size, shape, number and embryological origin (Leopold, 1976; Chapman, 1998; Özyurt et al., 2013a; Özyurt et al., 2013b). In most insects, their main function is the formation of seminal fluid and a spermatophore, which is vital for the transfer of sperm. Also the accessory glands are responsible for spermatophore production and produce some active peptides (Chen, 1984; Kaulenas, 1992; Davey and Krieger 1985; Freitas et al., 2010; Uceli et al., 2011). Male A. amygdali has a pair of accessory glands, which open into the vas deferens and the ductus ejaculatorius. These accessory glands are similar to those in D. baccarum and G. lineatum (Heteroptera: Pentatomidae) (Özyurt et al., 2013a; Özyurt et al., 2013b). However, Triatoma rubrofasciata (De Geer) and A. gabrieli Carvalho have only four accessory glands, and T. brasiliensis Neiva as well as T. melanica Neiva and Lent (Hemiptera: Reduviidae) have eight accessory glands. As a result of present study, these goals are followed: a) contribute to the knowledge of the male reproductive system of Pentatomidae; b) reveal the characters that may be useful for future studies; c) obtain the key information for future research into in the reproductive biology, ecology and biological control agents of the Heteroptera.

Literature Cited Adams, S. 2001. Morphology of the internal reproductive system of the male and female two-spotted stink bug, Perillus bioculatus (F.) (Heteroptera: Pentatomidae) and the transfer of products during mating. Intervertebrate Reproduction and Development 39(1):45-53. http://dx.doi.org/10.1080/07924259.2001.9652466 Life: The Excitement of Biology 2(1) 40

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Nijhout, H. F. 1994. Insect Hormones. Princeton University Press. Princeton, New Jersey, USA. 280 pp. Ozyurt, N., S. Candan and Z. Suludere. 2013a. The morphology and histology of the male reproductive system in Dolycoris baccarum Linnaeus 1758 (Heteroptera: Pentatomidae) Light and scanning electron micoscope studies. Micron 44:101-106. http://dx.doi.org/10.1016/j.micron.2012.04.017 Ozyurt, N. S. Candan, Z. Suludere and D. Amutkan. 2013b. Reproductive system in Graphosoma lineatum (Heteroptera: Pentatomidae) based on optical and scanning electron microscopy. Journal of Entomology and Zoology Studies 1(4):40-46. Papáček, M. and T. Soldán. 2008. Structure and development of the reproductive system in Aphelocheirus aestivalis (Hemiptera: Heteroptera: Nepomorpha: Aphelocheiridae). Acta Entomologica Musei Nationalis Pragae 48(2):339-338. Pendergrast J. G. 1956. The male reproductive organs of Nezara viridula with a preliminary account of their development (Heteroptera; Pentatomidae). Transactions of the Royal Society of New Zealand 84(1):139-146. Pires, E. M., P. S. F. Ferreira, R. N. C. Guedes and J. E. Serrao. 2007. Morphology of the phytophagus bug Platyscytus decempunctatus (Carvalho) (Heteroptera: Miridae). Neotropical Entomology 36(4):510-513. http://dx.doi.org/10.1590/S1519-566X2007000400004 Ramamurty, P. S. 1969. Histological studies of the internal organs of reproduction in Nezara viridula Fabr. Pentatomidae: Heteroptera, Insecta. Zoologischer Anzeiger 183:119-139. Rodrigues, A. R. S., J. E. Serrao, V. W. Teixeira, J. B. Torres, and A. A. Teixeira. 2008. Spermatogenesis, changes in reproductive structures, and time constraint associated with insemination in Podisus nigrispinus. Journal of Insect Physiology 54(1):1543-1551. http://dx.doi.org/10.1016/j.jinsphys.2008.09.003 Schaefer, W. C., Panizzi, A. R., 2000. Heteroptera of Economic Importance. CRC Press, LLC. Boca Raton, Florida, USA. 824 pp. http://dx.doi.org/10.1201/9781420041859 Schuh R. T. and J. A. Slater. 1995. True bugs of the world (Hemiptera: Heteroptera): Classification and Natural History. Cornell University Press, Ithaca, NY, USA and London, England, UK. 336pp. Uceli, L. F., V. D. Pirovani, N. M. F. Vicente, T. G. Pikart, P. S. F. Ferreira, and J. E. Serrão. 2011. Morphology of the reproductive and digestive tracts of Adparaproba gabrieli (Heteroptera: Miridae). International Journal of Tropical Insect Science 31(4):219-224. http://dx.doi.org/10.1017/S1742758411000385 Wieczorek K. and P. Swiatek. 2009. Comparative study of the structure of the reproductive system of dwarfish males of Glyphina betulae and Anoecia corni (Hemiptera, Aphididae). Zoologischer Anzeiger 248 (3): 153-159. http://dx.doi.org/10.1016/j.jcz.2009.04.001

Adult Apodiphus amygdali (Germar, 1817) (Heteroptera: Pentatomidae). Image from http://upload.wikimedia.org/wikipedia/commons/7/71/Apodiphus_amygdali_(Shieldbug_ sp.), Skala_Kalloni,_Lesbos,_Greece.jpg Life: The Excitement of Biology 2(1) 42

A review of the status of the larval parasitoid, Asecodes hispinarum Boucek, and of the pupal parasitoid, Tetrastichus brontispae Ferriere (Hymenoptera: Eulophidae), as biological control agents of the coconut leaf beetle, Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae: Cassidinae), in the Asia-Pacific Region1

He Liansheng2, Zuria Mohama Din2 and Yap Mei Lai2

Key Words: Asecodes hispinarum, Tetrastichus brontispae, Hymenoptera, Eulophidae, biological control, Brontispa longissima, Coleoptera, Chrysomelidae

Abstract: The Coconut Leaf Beetle, Brontispa longissima, endemic to Indonesia and Papua New Guinea, has spread to many countries in Asia and the Pacific region, where it has become a serious pest. Several countries have achieved significant control of B. longissima by releasing and establishing parasitoids, such as Asecodes hispinarum and Tetrastichus brontispae, which attack immature stages of the pest. A review of previous works undertaken on the biological control of the Coconut Leaf Beetle in these countries and elsewhere indicate that a combined release of A. hispinarum, with T. brontispae is an excellent tool to control B. longissima. Biological control of B. longissima is also seen to be environmentally sound and cost effective.

Introduction The Coconut Leaf Beetle, Brontispa longissima (Gestro) (Coleoptera: Chrysomelidae: Cassidinae: Hispines: Tribe Cryptonychini Chapuis: Brontispa Sharp) (Staines, 2012) is one of the most damaging pests of coconut, Cocos nucifera L. This species, which has been reported on several species of palms (Arecaceae) (Staines, 2012), is also known as the Two-coloured Coconut Leaf Beetle or the Coconut Hispine Beetle. The larvae and adults feed on the tissues of developing and unopened leaves of palm trees. This hispid beetle can cause significant production loss, and high infestation may result in the death of the trees (Kalshoven, 1981; Liebregts and Chapman, 2004). Damage to palms is followed by substantial yield loss. A study by the Food and Agriculture Organization (FAO) of the United Nations showed that, if left uncontrolled, the damage would be in excess of US$40 million annually in Vietnam alone (Liebregts and Chapman, 2004). Brontispa longissima is believed to be endemic to Indonesia, Papua New Guinea and possibly also to Malaysia (FAO, 1981; Liebregts and Chapman,

1 Submitted on July 4, 2013. Accepted on July 15, 2014. Last revisions received on May 12, 2014. 2 Plant Health Laboratory Department, Laboratories Group, Agri-Food and Veterinary Authority of Singapore, Singapore 718827. E-mails: [email protected], [email protected] , [email protected] , respectively.

DOI:10.9784/LEB2(1)He.01 Electronically available on May 16, 2014. Mailed on May 14, 2014. Life: The Excitement of Biology 2(1) 43

2004). In recent years, the species has become widespread in South East Asia and the Pacific region. Outside its presumed native range, it was first detected in the Mekong Delta in Vietnam in the late 1990’s (Liebregts and Chapman, 2004). The geographical distribution of B. longissima is illustrated in Rethinam and Singh (2007), Nakamura et al. (2012), and CABI (2014). Two mitochondrial clades of B. longissima, each with different life history traits, are discussed in Nakamura et al. (2012, see also references therein for more details). Chemical control of this pest has been extensively studied. Several insecticides including imidacloprid, chlorfenvinfos, diazinon, and carbofuran were used to combat the Coconut Leaf Beetle (Baringbing and Karmawati, 1992; He et al., 2006). However, the effects of those treatments last only from several days to several weeks depending on the property of pesticides and the methods of application. In addition, chemical control substantially increased costs and threatened the ecosystem. Until 2004, this invasive pest did not have adequate natural enemies to suppress its populations in Southern East Asia. Historically, biological control has been used primarily on exotic pests (Grandgirard et al., 2008; Hall et al., 1980; Hall and Ehler, 1979). Hence, the biological control of B. longissima was considered a good approach to tackle this pest.

Biological control as a pest control measure Biological control is an effective control method for pestiferous insects, mites, weeds and plant diseases, using other living organisms (Flint and Dreistadt, 1998). A compelling motivation for adoption of biological control is the reduced ongoing expenditure for pesticides, labour, specialized equipment and potentially a permanent return to ecological conditions (Norgaard, 1988, Pickett et al., 1996; Jetter et al., 1997). Biological control of arthropod pests becomes an important component of cost effective, environmentally benign integrated pest management (Gurr et al., 2000). Based on the biological control agents used, there are broad sense biological controls and classic biological controls. In the broad sense, biological control is any action of one organism against another. This approach to biological control embraces the use of natural ‘macrobial’ and ‘microbial’ agents (Huffaker, 1977, van Lenteren et al., 2006a). Many biological control schemes use predatory insects and mites, insects that parasitize other insects (parasitoids) or nematodes, targeted against insect and mite pests; these are the so-called ‘macrobial’ agents. There are also various ‘microbial’ agents (bacteria, viruses and fungi) that have been developed and applied for arthropod biological control programs (van Lenteren and Woets, 1988; van Lenteren, 2003; van Lenteren et al., 2006a, 2006b). In its narrow sense, biological control has meant a planned introduction of a biological agent that may reduce a pest problem (Huffaker, 1977). Narrow sense biological control has been applied to combat insect pests for more than hundred years, and includes classical biological control (CBC) and Life: The Excitement of Biology 2(1) 44

augmentative biological control (ABC) (van Lenteren, 2000, 2003; van Lenteren et al., 2006a). Classical biological control of insects, in which exotic natural enemies are introduced to control exotic pests, has been applied for more than 120 years and the release of more than 2,000 species of natural enemies have resulted in the permanent reduction of at least 165 pest species worldwide (Greathead, 1995; Gurr and Wratten, 2000). In contrast, augmentative biological control, in which exotic or native natural enemies are periodically released, has been used for close to 90 – 100 years with more than 150 species of natural enemies available on demand for the control of about 100 pest species (van Lenteren, 2003). Contrary to the thorough environmental risk evaluations applied in the search for natural enemies of weeds (Blossey, 1995; Lonsdale et al. 2001, Wapshere, 1974), potential risks of biological control agents for arthropod control has not been routinely studied in pre-release evaluations (van Lenteren and Woets, 1988; van Lenteren et al., 2003), with the exception of several CBC programmes for which accurate non-target species testing has been used (Barratt et al., 1999; Neuenschwander and Markham, 2001). Until now, very few problems have been reported concerning negative effects of release of arthropods for the control of pestiferous arthropods (Lynch et al., 2001), despite more than 5,000 introductions in at least 196 countries or islands (Greathead, 1995, Gurr and Wratten, 2000; van Lenteren, 2000, 2003). This suggests the safety of biological control approaches. However, insect pest management with biological control is undergoing dramatic change due to heightened awareness of non-target impacts and increasing scrutiny by regulatory agencies. Discussions on the risk of release of exotic natural enemies for non-target species took a prominent place in biological control programs. Retrospective analyses of biological control projects have provided quantitative data on non- target effects and illustrated the need for risk assessments to increase the future safety of biological control (Louda et al., 2003, Lynch et al., 2001). In this review, the terminologies related to biological control and environmental risk assessments (ERA) have been taken from recent publications in this area [Convention on Biological Diversity (CBD), 2002; Eilenberg et al., 2001; International Plant Protection Convention (IPPC), 2005; van Lenteren, 2006)]. Thus far, very few negative reports of pest risk analysis (PRA) or ERA are found for either CBC or ABC (Greathead, 1995; Gurr and Wratten, 2000; van Lenteren, 2000, 2003). In the past several years, classic biological control of B. longissima by introducing exotic wasps was extensively studied and widely adopted (Wood, 2002; CFC/DFID/APCC/FAO, 2004; Chen et al., 2010; Liebregts et al. 2006; Liu et al. 2008; Lu et al. 2005a, 2005b, 2006; Sun et al., 2011; Tang et al., 2006, 2007a, 2007b; Pundee, 2009; Xu et al., 2008). A literature review was carried out to better understand how to control the coconut hispid using parasitoid wasps in South East Asia. The foci of the search were parasitoid wasps in the Life: The Excitement of Biology 2(1) 45

family Eulophidae that attack the larval or pupal stages of B. longissima. This search included the larval parasitoid Asecodes hispinarum and the pupal parasitoid Tetrastichus brontispae.

Biological control of B. longissima Biological control by using parasitoids, predators and entomopathogenic fungi has been shown to reduce the field population of B. longissima (Meldy et al., 2004). Natural enemies that attack only during one stage of the pest may not achieve satisfactory control of B. longissima; observations from South Sulawesi showed that the pest had overlapping generations (Meldy et al., 2004). The parasitoid complex of B. longissima comprised parasitoids of eggs, larvae and pupae (Hollingsworth et al., 1988). The common egg parasitic wasps were Haeckeliana brontispa Ferriere, Trichogrammatoidea nana Zehntner (both Hymenoptera: Trichogrammatoidae) and species of Ooencyrtus (Hymenoptera: Encyrtidae). The parasitoid of the larvae, A. hispinarum, and parasitoid of pupae, T. brontispae, were reported to be common and effective (Lever, 1969). After scrupulous screening, those two parasitoids were selected as biocontrol agents to combat B. longissima by FAO (FAO, 2004). To facilitate the biological control of coconut hispids, FAO conducted a Technical Cooperation Programme (TCP) during 2003-2005 in Vietnam, Nauru (located in the Pacific Ocean), and Maldives (located in the Indian Ocean). Under this project, collection of the parasitoid A. hispinarum from Samoa and its subsequent introduction in these countries was conducted. Initial surveys confirmed the establishment of the parasitoid in Vietnam and Maldives, where observations showed that damage to young emerging leaves was reduced. The Vietnam project showed a return on investment of US$3,000 for every dollar invested by FAO (FAO, 2004). Since then, successful control of B. longissima with high cost/benefit ratios has been achieved in several other countries by importing and establishing the two parasitoids that attack immature stages of the Coconut Leaf Beetle. The successful locations included Celebes (Indonesia), Tahiti, Solomon Islands, Western Samoa (Volgele, 1989), Taiwan (Chiu and Chen, 1985), Vietnam (Viet, 2004) and China (Li et al., 2008). Many other countries, including Thailand and Maldives, are actively mass rearing and releasing the two species of parasitic wasps against B. longissima (FAO, 2004; Fu and Xiong, 2004; Htwe et al., 2013; Pundee et al., 2009; Shafia, 2004; Sindhusake and Amporn, 2004).

Characteristic attributes of A. hispinarum and T. brontispae relevant to the success or failure of biological control Understanding the characteristic attributes of biological control agents is very important to the success or failure of releases. Through retrospective analysis, it is clear that there are situations where arthropod biological control agents have been successful and other situations where they have failed to Life: The Excitement of Biology 2(1) 46

impact the target pest species. In other situations, biological control agents have backfired, causing more harm than good (Greathead, 1986; Hunt et al., 2008). Studying the attributes associated with effective biological pest control and high environmental adaptability of the biocontrol agents would help in selecting potentially successful biological control projects (Berkvens et al., 2009; Haye et al., 2009; Murray et al., 2009). Murdoch (1994) summarized a principle hypothesized to govern the effectiveness of specialized biological control agents. Agents that can persist when their prey items or host populations are very low in number should be favoured, assuming other traits equal. In addition, a number of authors have analyzed the historical record of biological control agents to identify factors or traits that are associated with success and failure (Hawkins et al., 1993; Hawkins and Cornell, 1994). Table 1 below highlights the successful attributes of some biological agents.

Table 1. Attributes that contributed to the success of biological control.

Target pest Biological Attributes species agent used  Thermal tolerance Rodolia Icerya purchasi cardinalis  Short development time with respect to prey Maskell (Mulsant) (DeBach and Quezada,1973)

 High dispersal ability Trialeurodes Encarsia  High searching ability vaporariorum formosa Gahan (Westwood)  Accepts all immature host stages  Ease of mass rearing (van Lenteren, 1995)  Voracious feeding  High dispersal ability Phytoseiulus Tetranychus persimilis  High searching ability urticae Koch Athias- Henriot  Ease of mass rearing  Availability of pesticide resistant strain (van Lenteren, 1995)  Attack of early host instars Phenacoccus Apoanagyrus  Production of more females on young hosts manihoti lopezi De  Superior competitive ability Matile-Ferrero Santis  High search capacity (Neuenschwander, 2001)

Biology and mass rearing of the larval parasitoid, A. hispinarum has been conducted under laboratory conditions by several authors in various countries (Sindhusake and Amporn, 2004; Htwe et al., 2013; Lu et al., 2005a, 2005b, Life: The Excitement of Biology 2(1) 47

2008; Sun et al., 2011; Tang et al., 2006, 2007a, 2007b; Pundee, 2009; and Viet, 2004). In 2006, the mass rearing of both species of wasp was initiated in the Entomology and Nematology laboratory, Plant Health Laboratory Department, Agri-Food and Veterinary Authority of Singapore (AVA). Laboratory populations of these two species were established and mass rearing protocols developed (AVA, 2011, unpublished report). The characteristics of these two species were found to be similar to those reported under laboratory conditions. Attributes of T. brontispae and A. hispinarum relevant to success or failure of releases for pest biological control are summarised in Table 2. Qian et al. (2011) released A. hispinarum and T. brontispae simultaneously in the same locations to control B. longissima. The results indicated that B. longissima was most effectively controlled when there were 40 - 60 A. hispinarum and 10 - 20 T. brontispae in each container (the ratio of T. brontispae to A. hispinarum was approximately one to four).

Table 2. Characteristic attributes of T. brontispae and A. hispinarum relevant to the success or failure of biological control.

Important Asecodes hispinarum Tetrastichus brontispae attributes  At 22 °C, A. hispinarum  Optimum temperature at 20 - adults’ survival was the 28 °C with parasitic ratio longest (Lu et al., 2005a, reached 95% (Chen et al., 2005b; Tang et al., 2007a, 2010). 2007b and Pundee, 2009).  When temperature was below  The effective temperature 18°C, parasitic ratio was 52.2% range was from 16 - 32 °C and when above 30 °C, it was Response to (Tang et al., 2007a). 69.5% (Chen et al., 2010). temperature  The highest parasitic efficiency was at 28 °C (Tang et al., 2007a).  Temperature had no effect on the sex ratio of the parasitoid offspring (Lu, 2008).  When fed with 10% honey  When fed with 10% honey (v/v), the average longevity (v/v), the longevity of the wasp of the wasp was 4.9 days was 13.4 days (Huang et al., (Pundee, 2009). 2007). Adult longevity  The longest mean developmental time was 23.8 days while the shortest was 16.5 day at 28 °C (Htwe et al., 2013). Life: The Excitement of Biology 2(1) 48

 43 eggs/female (Lu et al.,  53.6 eggs/female (Huang et al., Fecundity 2005a) to 47.3 eggs / female 2007). (Pundee, 2009).

 The larvae of Plesispa  Pupae of B. longissima (Ding et reichei and B. longissima al., 2007). but the latter was preferred  Females of T. brontispae could (Sindhusake and Amporn, parasitize pre-pupae and 1 to 5- 2004; Pundee, 2009). day-old pupae but 1-day pupae Host range  The 3rd and 4th instars preferred (Chen et al., 2010). larvae of B. longissima were the best host stages for mass production (Htwe et al., 2013; Pundee, 2009; Viet, 2004).

 16 – 23 days (Htwe et al.,  17.1 – 46.2 days (Chen et al., Life cycle 2013). 2010).

 The hunting time of A.  The parasitized rates on pupae hispinarum was not affected of B. longissima reached at by change of temperature 72% to 92.78% on 45 days after range of 16 °C to 28 °C releasing (Ding et al., 2007). (Tang et al., 2007a).  6 months after release, B.  The percentage of longissima per tree decreased parasitized B. longissima between 3.3 to 44.3 times the larva increased with the original population size (Ding increase in host density et al., 2007). (Tang et al., 2007b).  The dispersal distance was Behaviour  The peak ovi-position was around 10-50 metres 20 days within 12 hours after mating after field release. (Lu et al., 2005b).  The longest dispersal distance  The optimal time for was 6.06 km, seven months parasitisation was at 24 after release (Ma et al., 2006b). hours after emergence of adults (Pundee, 2009).  The parasitization efficiency decreased with the increase in A. hispinarum density (Lu et al., 2005b).

Asecodes hispinarum as a biological control agent Asecodes hispinarum was reported to have originated in Papua New Guinea (Boucek, 1988; Voegele, 1989). This parasitoid was successfully introduced into Life: The Excitement of Biology 2(1) 49

Samoa in the early 1980's for the control of B. longissima (Volgele and Zeddies, 1990). Asecodes hispinarum was reported to be the only biological control agent that controlled the pest in Western Samoa during the 1980’s. In the last thirty years, A. hispinarum has played a very important role in the control of the Coconut Leaf Beetle with no negative effects (Volgele and Zeddies, 1990). In 2003, FAO collected the parasitoid A. hispinarum from West Samoa and this parasitoid was identified as the main biological control agent of coconut hispids for their Technical Cooperation Projects (TCP). These were later introduced into southern Vietnam and other Asian countries to control B. longissima (FAO, 2004). In Vietnam, these tiny wasps were first reared in containment facilities and released in 15 provinces of south and central Vietnam (Viet, 2004). Early observations indicated that the effectiveness of the parasitoids was likely to be affected by the prevailing environmental conditions where they were relased. In view of this, FAO organized a research group to strengthen the biological control programme, and completed exploratory surveys in Indonesia, Papua New Guinea and the Solomon Islands. Results of field surveys indicated that the parasitoids spread at the rate of 5-8 km in two months and, within four months, 60-90% recovery of palms was observed (FAO, 2004). In Vietnam, it was expected that the damage levels would be reduced to levels similar to those seen in Samoa, where B. longissima damaged palms were uncommon after the release of the parasitoids (Viet, 2004). In the Maldives, the parasitoids established within two months after initial field releases in February 2004. The newly emerging leaves appeared to show less damage, although statistically significant reduction in damage was not observed. This reduction could be attributed to the impact of the parasitoids (Shafia, 2004). China organized a group of experts to study the biological control of the Coconut Leaf Beetle using A. hispinarum in Vietnam (Fu and Xiong, 2004). Asecodes hispinarum was subsequently brought to Hainan, China, in March 2004 and after appropriate risk assessment, it was released in Hainan Province, China. To evaluate the potential efficacy of this parasitoid in Hainan, under containment conditions, a series of relevant research was conducted to study the morphology, development, behavior, biological parameters due to temperature, feeding and host range of this species (Table 2). Asecodes hispinarum consignment did not bring dangerous microbes and parasites, and the wasps did not parasitize other important native insects, such as ladybird beetles, silkworms, honeybees, and moths (Fu and Xiong, 2004). Therefore, A. hispinarum must be a monophagous or oligophagous insect (Sindhusake and Amporn, 2004; Pundee, 2009). No negative impact to the environment, economy or ecology was observed (Fu and Xiong, 2004; Sindhusake and Amporn, 2004; Pundee, 2009) by its release and this corroborates our observations in Singapore (AVA, 2011 unpublished report). Life: The Excitement of Biology 2(1) 50

After a safety evaluation, A. hispinarum has been released in the north (Haikou), the south (Sanya) and the east (Qionghai) of Hainan, China, since August 2004. A primary survey to study the efficacy of the released natural enemy found that the number of Coconut Leaf Beetles decreased greatly, the infested trees recovered to a certain degree, and the parasitisation rate was 10- 40% (Fu and Xiong, 2004). The effects of different larval instars of the beetle on parasitism, and the influences of temperature and humidity on development of A. Hispinarum, were also investigated. Under laboratory conditions (24° C ± 2° C and RH 75% ± 10%), the mean developmental duration of egg, larva and pupa were 2.8 days, 6.7 days and 7.5 days, respectively; the longevity of adults without nutritional supplements was 2.5 days on average. Both the temperature and nutritional supplement affected the longevity of adults, and the mean longevity of adult females was longer than that of adult males. Fecundity (per female) was 43 on average and the peak of oviposition occurred within 12 hours after mating. The functional response of A. hispinarum to 4th instar larvae of B. longissima belonged to Holling's type II and the parasitisation efficiency of A. hispinarum decreased with increase in A. hispinarum density (Fu and Xiong, 2004; Lu et al., 2005). Biological control in Vietnam showed huge benefits in the cost-benefit analysis. By mid 2002, around 9.4 million trees were infested by B. longissima and until mid 2004, the pest infestation had caused 30% loss in fruit production, death of 5% of trees (at an estimated cost of US$23.8 million) and had also damaged 13,000 ornamental palms at an estimated cost of US$838,000 (FAO, 2004; Viet, 2004). The cost of pesticide applications amounted to approximately US$715,000, which was borne by the federal and provincial governments. This cost did not include the labour undertaken by the farmer volunteers involved in the control programme. Overall, the cost of FAO -TCP (US$350,000) was very small when compared to the losses caused by B. longissima. Using a unit price of US$0.10 per coconut (including husk), a tentative analysis of various economical data points was conducted, predicting returns of one billion dollars over a 30-year period or returns of US$2,000-3,000 for every dollar invested in the project (Viet, 2004). Apart from Vietnam, China, Maldives and Nauru (located in the Pacific Ocean), A. hispinarum was also found to be successful controlling B. longissima in Thailand, Cambodia, Laos, and Indonesia (Boucek, 1988; Shafia, 2004; Sindhusake and Winothai, 2004; Viet, 2004; Volgele, 1989). In addition to the reports from China (Fu and Xiong, 2004), researchers in Thailand and Vietnam also did not encounter A. hispinarum parasitizing larvae of darkling beetles, Tenebrio molitor Linnaeus (Coleoptera: Tenebrionidae); lady bird beetles, Hippodamia convergens Guérin-Méneville (Coleoptera: Coccinelllidae); the common cutworm, Spodoptera litura (Fabricius) (Lepidoptera: Noctuidae); or lacewings, Mallada basalis (Walker), Chrysoperla carnea (Stephens) (the latter two Neuroptera: Chrysopidae) (Sindhusake and Life: The Excitement of Biology 2(1) 51

Winothai, 2004; Viet, 2004). Results of host range studies further confirmed that A. hispinarum was a monophagous or oligophagous parasitoid (Sindhusake and Winothai, 2004). The wasps would automatically disappear once their hosts vanished. Therefore, A. hispinarum is considered quite safe to non-target insects as well as plants.

Tetrastichus brontispae as a biological control agent Ferriere (1933), considered Tetrastichus brontispae a main natural enemy of B. Longissima, as it parasitizes the larval and pupal stages. Tetrastichus brontispae was found to be native to Java, Indonesia (Kalshoven, 1981; Lever 1969; Meldy et al., 2004; Tjoa, 1953). Studies on the use of T. brontispae as a pupal parasitoid have been carried out by many researchers (Kalshoven, 1981; Lever, 1969; Tjoa, 1953, 1965). There is a long history in the use of the wasp, T. brontispae, as a biocontrol agent. The earliest application of T. brontispae against B. longissima was as early as 1920 in Indonesia (Leefmans, 1935; Lever 1936a, 1936b). Leefmans (1935) demonstrated that T. brontispa was the most effective biological agent against B. longissima. Other studies also indicated that T. brontispa had high potential as a biological control agent of the hispids. It was reported that this parasitoid efficiently controlled the pupae of B. longissima both in the laboratory as well as in the field. The percent of parasitization under laboratory conditions and in the field ranged from 76 - 87% and 35 - 74 % respectively. These results demonstrated the high potential of T. brontispa as a biological control agent against B. longissima (Meldy et al., 2004). The introduction of T. brontispae against B. longissima in Sulawesi (formerly known as Celebes) started in 1932 (Meldy et al., 2004). Within three years, around 37,500 parasitized pupae were sent from Bogor to Makassar (Ujung Pandang). Eventually, ten rearing stations were established over South Sulawesi, and a total of around 13 million parasitized pupae were released between 1935 and 1941 in various locations. The rate of parasitization among field-collected pupae was between 70 - 90%. After a gap of 5 years, it was between 20 and 40%. In 1948-1949, the rate of parasitization reached ca. 40% in the 20 locations surveyed (Franssen and Tjoa, 1952). The establishment of T. brontispae brought B. longissima under control. The eulophid T. brontispae was found to parasitize around 60-90% of the pupae and around 10% of the larvae of B. longissima (Kalshoven, 1981; Tjoa, 1953). About 20 wasps emerged from one B. longissima pupa in around 18-days (Chiu et al., 1988, Tjoa 1953). Hyperparasitoids had not yet been observed on any T. brontispa (Kalshoven, 1981, Tjoa; 1953; Lever, 1969). Tetrastichus brontispa parasitizing the hispids in Pakuwon (West Java), Central Java and South Sulawesi was around 36.4%, 11.1% and 50.6, respectively. The level of parasitization was considered lower than that reported by Kalshoven (1981), who reported parasitization of 10% for larvae and 60-90% Life: The Excitement of Biology 2(1) 52

for pupae. The differences could have been due to environmental conditions in every location, insects and plant biodiversity (Kalshoven, 1981). On Banika Island (Russell Group, located in the Pacific Ocean), T. brontispae was first released against B. longissima in 1936 (Lever, 1937). In 1938, it was reintroduced in the Solomon Islands without controlling the Coconut Leaf beetle. Another introduction in 1968 succeeded and the parasitoid spread over 100 acres by the end of 1969, with effective control achieved and 70% parasitization. The parasitoid spread rapidly and greatly reduced the infestation (Stapley, 1973, 1979). This wasp was also imported to Rabaul (New Britain in Papua New Guinea) from the Solomon Islands in 1936. Large numbers were released near Rabaul and parasitized pupae were recovered (O'Connor, 1940; Froggatt and O'Connor, 1941). On Saipan (Philippine Islands) and Rota Island (located in the Pacific Ocean), T. brontispae, obtained from Java, were released in 1948 for the control of B. longissima. The parasitoids appeared to be well established by 1954, sometimes providing parasitization of up to 90 % (Stapley, 1971, 1973, 1979). The rearing and release of the pupal parasitoid T. brontispae for the control B. longissima was recommended as an important hispid beetle management measure (Stapley, 1979). Tetrastichus brontispae was introduced into the Noumea Peninsula, New Caledonia where it became established. However, the rate of parasitization did not exceed 24%, and even a combination with fungal diseases did not reduce the incidence of the pest to a satisfactorily low level, though no negative effects were observed (Cochereau, 1969). In 1974, T. brontispae was introduced into Guam, New Hebrides, New Caledonia and the Solomon Islands with shipments from Saipan. The parasitoids became established and in the early 1980s, rates of parasitization ranging from 2 to 72 % in different locations were reported (Muniappan et al., 1980). In Darwin, Australia, T. brontispae was imported from New Caledonia as a biological control agent against B. longissima in 1982 (Chin and Brown, 2001; Halfpapp, 2001) when it was first detected in 1979. The initial introduction was not successful, but a new introduction in 1984 established the wasps for five years before they disappeared (Halfpapp, 2001). Tetrastichus brontispae was reintroduced in Darwin in 1994 and established in moderate numbers for almost two years. Between October 1994 and March 1997, the beetle damage to the coconut palms was reduced by 20% at the sites where T. brontispae was released. The parasitoid became established in larger population at sites that were irrigated with overhead sprinklers. After November 1996, the numbers of T. brontispae diminished and the wasp could not be collected from any of the release sites or nearby areas. The climate at the northern tip of the Northern Territory may have been responsible for the parasitoid’s failure to become established, as T. brontispae is probably better suited for a milder tropical climate (Chin and Brown, 2001). Only in North Queensland did the release of T. Life: The Excitement of Biology 2(1) 53

brontispae demonstrate effective control of B. longissima. From the Australian experience, it was reported that successful releases were dependent on the initial release of large numbers of T. brontispae (Halfpapp, 2001). In Samoa and American Samoa, T. brontispae have been mass-released since 1981 for the long-term control of B. longissima. From 1984 to 1987, a steady decline in damage was observed after the release of T. brontispae as well as the larval parasitoid, Asecodes sp. (Volgele and Zeddies, 1990). The incidence of palms damaged by B. longissima in plantations and villages was 4 and 22.9% respectively (Volgele and Zeddies, 1990). In American Samoa approximately 74 % of all the palms were infested, compared with only 14.3 % in Samoa. Damage to the total leaf area of coconut palms by B. longissima was 10% in American Samoa and only 1–2% in Samoa. A survey revealed that Asecodes sp. was an important cause of larval mortality in Samoa whereas no parasitoids were found in American Samoa (Volgele and Zeddies, 1990). An extensive survey of the 37,000 damaged trees in Western Samoa showed that B. longissima was under control and did not cause any significant yield losses (initial production losses were estimated to be as high as 50 – 70%). Since 1954, biological control has been a primary method of pest management in American Samoa (Tauili'-ili and Vargo, 1993). Ten releases of a total of 11,456 T. brontispae adults were made from January to July 1984 in Chenchinhu, Taiwan, and seven releases of 4,881 parasitoids were made from February to June 1984 in Linbien, Taiwan. The percentage parasitisation of pupae recorded from field recoveries at the two sites were 21 - 79% and 9 - 36%, respectively. The parasitoid prevented most host larvae from developing into adults at Chenchinhu, whereas at Linbien, the chrysomelid populations were not effectively suppressed (Chiu and Chen 1985). The parasitoid had established at distances of up to 2 - 8 km from the release site at Chenchinhu (Chiu et al., 1988). The establishment of T. brontispae as a biological control agent of B. longissima in Taiwan was confirmed by Chiu et al. (1988). Tetrastichus brontispae was introduced to Hainan, Mainland China, from Taiwan in 2004 (Fu and Xiong, 2004). According to Heroetadji (1989), the parasitoid, T. brontispae parasitizes the larvae and pupae of Plesispa reichei and P. nipae as well as B. longissima. No negative effects were reported in countries where T. brontispae was released for hispid control in the last 50 years. The application of A. hispinarum and T. brontispae against B. longissima by different countries/regions is summarised in Table 3.

Life: The Excitement of Biology 2(1) 54

Table 3. The application of Asecodes hispinarum and Tetrastichus brontispae against Brostispa longissima for biological control by different countries/regions.

Year of B. Country Infestation of palm trees longissima Biological control and losses incurred invasion China 2002 The beetle occurred in 16 Asecodes hispinarum counties of Hainan and entomopathogenic province, infested about fungus Metarhizium 817, 000 trees and anisopliae were tested. endangered around 40,000 Asecodes hispinarum hectares (FAO 2004, Fu had been released in the and Xiong 2004). north (Haikou), the south (Sanya) and the east (Qionghai) of the island since August 2004. Parasitization rate of 10-40 % was recorded. Tetrastichus brontispae was introduced from Taiwan and the studies to use them as biological control agent are in progress (Fu and Xiong, 2004).

Indonesia 1983 Brontispa longissima Pupal parasitoid (T. recorded in West and brontispae), Central Java, S.E. Sulawesi, entomopathogenic fungi Bali, etc (FAO, 2004; Meldy (Metarhizium et al., 2004). anisopliae var. anisopliae and Beauveria bassiana) were used. Under field conditions, 35.7 to 73.6 % parasitisation of the hispid was achieved (Meldy et al., 2004).

Lao PDR 2001 Infestation and damage in Asecodes hispinarum People's six villages within two was introduced and Democratic provinces (Khennavong, released (Khennavong, Republic 2004). 2004).

Life: The Excitement of Biology 2(1) 55

Maldives 1999 On Sun Island resort, The parasitoid, A. Nalaguraidhoo and hispinarum, was reared, in South Ari Atoll (Shafia, released and established 2004 ). in Maldives (Liebregts and Chapman, 2004; Shafia, 2004).

Thailand 2000 Infestation of 7229 hectares Rearing of A. worth US$30 million of hispinarum in August production affecting around 2004 for release 50,000 smallholder farmers (Sindhusake and (Sindhusakeand Winothai, Winothai, 2004). 2004).

Vietnam 1999 Losses estimated at The parasitoid, A. US$17.8 million to the hispinarum, was reared, coconut industry in 2002 released and established (Viet, 2004). in Vietnam (Liebregts and Keith, 2004; Viet, 2004).

Conclusions and Recommendations The Coconut Leaf Beetle, B. longissima, an endemic pest in Indonesia and Papua New Guinea, has devastated palms in many countries in and outside this region. Controlling this pest using natural enemies has proved effective. A literature review has indicated that B. longissima could be successfully brought under sustainable control by applying environmentally friendly classical biological control agents, such as Asecodes hispinarum and Tetrastichus brontispae, as shown in many Southeast Asian and Pacific countries. Complete control of B. longissima with high cost/benefit ratio was achieved in several countries by importing and establishing parasitoids that attacked immature stages of the pest. The larval parasitoid A. hispinarum, collected and introduced in Vietnam, Maldives and Nauru to combat the beetle was quite successful in reducing the population of coconut hispids, resulting in great economic benefit. Other successful locations included some Pacific Islands, as well as East and Southeast Asian countries. The wasps are now being reared and released in Thailand, Laos, Cambodia, China, and Malaysia. As compared to A. hispinarum, T. brontispae employed as a biocontrol agent to combat coconut hispid beetles had a longer history and proved to be the most effective biocontrol agent against the coconut hispid beetles as early as 1920. The results of biological experiments involving the parasitoids showed that both A. hispinarum and T. brontispae had wide ranges of adaptation to temperature, thermal tolerance, short developmental time and highreproductive capacity. In addition, both A. hispinarum and T. brontispae had reasonable Life: The Excitement of Biology 2(1) 56

parasitic rates against their host insects (Chalerm and Amporn, 2004; Chen et al., 2010; Htwe et al., 2013; Liu et al. 2005 a, 2008; Lu et al., 2005b; Sun et al., 2011; Tang et al., 2006; Tang et al., 2007a, 2007b; Pundee, 2009; Viet, 2004). This literature review has revealed that A. hispinarum and T. brontispae have been used as biocontrol agents against B. longissima. Results of our observations in Singapore of more than 20 generations of A. hispinarum were not associated with any harmful microbes or other hyperparasitoids. With a very narrow host range and either monophagous or oligophagous, these parasitoids die off once the host population has reached a low threshold. Therefore, releasing these two parasitoids for control of B. longissima offers a safe and effective alternative with minimal impact to the environment. Natural enemies attacking only a single stage of the pest might not achieve satisfactory B. longissima control, as results from South Sulawesi indicated that the pest had overlapping generations. Hence better control would be envisioned when both the larval parasitic wasps, A. Hispinarum, and pupal parasitic wasps, T. brontispae are used concurrently as biological control agents against B. longissima. Parasitism commonly results in a unique array of host physiological responses and adaptations. These physiological changes are often manifested by altered host behaviour. The functional and evolutionary relationships between the two species of parasitoids and their host insects, hispid beetles, need to be studied further. Physiological effects may be assessed as to whether they affect fitness and confer benefit or harm to one or both of the symbionts involved. It would be useful if these physiological responses, specifically neural, endocrine, neuromodulatory and immunomodulatory components which may interact to modify host behaviours, are examined. Results of adaptation strategies of hispids to both parasitic wasps and host plants can vastly improve the efficacy of future hispid biological control programmes.

Acknowledgements The authors wish to express their appreciation to Dr. Varughese Philip and Dr. Mohamed Ali of Agri-Food & Veterinary Authority, Singapore for critically editing the manuscript.

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Stapley J. H. 1971. The introduction and establishment of the Brontispa parasite in the Solomon Islands. South Pacific Commission Information Circular 30:2-6. Stapley, J. H. 1973. Insect pests of coconuts in the Pacific region. Outlook on Agriculture 7(5):211- 217. Stapley, J. H. 1979. Notes on biological control in the Solomon Islands. IOBC (International Organisation for Biological and Integrated Control) Newsletter 1979(11/12):4-5. Sun, R.-F., X-Q. Tian, X.-M. Zhang, Y.-C. Li, F. Quan, and L. Zhu. 2011. Comparisons of the field and laboratory populations of Asecodes hispinarum Boucek. Chinese Journal of Applied Entomology 48(4):934-940. Tang, C., Z. Q. Peng, K. H. Wu, Y. J. Liang, Y. G. Fu, and F. H. Wan. 2006. The effect of sublethal doses of insecticides on the functional response of Asecodes hispinarum. Chinese Bulletin of Entomology 43(5):644-647. [in Chinese] Tang, C., Z. Q. Peng, Q.-A. Jin, Y. G. Fu, and F. H. Wan. 2007a. Effects of variable temperature on development of Asecodes hispinarum (Hymenoptera: Eulophidae). Acta Phytophylacica Sinica 34(1):1-4. [in Chinese] Tang, C., Z. Q. Peng, K. N. Chen, B. Q. Lu, Q. A. Jin, J. Zhou, Y.G. Fu, and F.H. Wan. 2007b. Influence of temperature on functional response of Asecodes hispinarum. Chinese Journal of Biological Control 23(1):11-13. [in Chinese] Tauili'-ili P. and R. M. Vargo. 1993. History of biological control in American Samoa. Micronesica Supplement 4:57-60. Tjoa, T. M. 1953. Memberantas hama-hama kelapa dan kopra. Noordhoff-Kolff. Jakarta, Indonesia. 270 pp. Tjoa, T. M. 1965. The occurrence of two strains of Brontispa longissima (Gestro) (Coleoptera: Hispidae) based on resistance or non-resistance to the parasite Tetrastichus brontispae (Ferr.) (Hymenoptera: Eulophidae) in Java. Bulletin of Entomological Research 55: 609-614. http://dx.doi.org/10.1017/S0007485300049713 van Lenteren, J. C. 1995. Integrated pest management in protected crops. pp. 311-343. In, Integrated Pest Management. Dent, D. and N. C. Elliott (Editors). Chapman and Hall. New York, NY, USA. 356 pp. van Lenteren, J. C. and J. Woets. 1988. Biological and integrated pest control in greenhouses. Annual Review of Entomology 33:239–269. doi:10.1146/annurev.en.33.010188.001323 van Lenteren, J. C. 2000. A greenhouse without pesticides: fact or fantasy? Crop Protection 19, 375–384. doi:10.1016/S0261-2194(00)00038-7 van Lenteren, J. C. 2003. Environmental risk assessment of exotic natural enemies used in inundative biological control. BioControl 48, 3–38. doi:10.1023/A:1021262931608 van Lenteren, J. C. 2006. How not to evaluate augmentative biological control. Biological Control 39:115–118. http://dx.doi.org/10.1016/j.biocontrol.2006.05.014 van Lenteren, J. C., J. S. Bal, F. Bigler, H. M. T. Hokkanen, and A. J. M. Looman. 2006a. Assessing risks of releasing exotic biological control agents of arthropod pests. Annual Review of Entomology 51:609–634. doi:10.1146/annurev.ento.51.110104.151129 van Lenteren, J. C., M. J. W. Cock, T. S. Hoffmeister, and D. P. A. Sands. 2006b Host specificity in arthropod biological control, methods for testing and interpretation of the data. pp. 38–63. In, Environmental impact of invertebrates for biological control of arthropods: methods and risk assessment. Bigler, F., D. Babendreier and U. Kuhlmann (Editors). CAB International. Wallingford, England, UK 299 pp. http://dx.doi.org/10.1079/9780851990583.0038 Viet, T. T. 2004. Classical biological control of coconut hispine beetle with the parasitoid Asecodes hispinarum Boucek (Hymenoptera: Eulophidae) in Vietnam. pp. 90-99. In, FAO (Food and Agriculture Organization of the United Nations). Report of the Expert Consultation on Coconut Beetle Outbreak in APPPC Member Countries. 26-27 October 2004. Bangkok, Thailand. 147 pp. http://www.fao.org/docrep/007/ad522e/ad522e00.htm Volgele, J. M. 1989. Biological control of Brontispa longissima in Western Samoa: an ecological and economic evaluation. Agriculture, Ecosystems and Environment 27:315-329. http://dx.doi.org/10.1016/0167-8809(89)90095-9 Life: The Excitement of Biology 2(1) 63

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Book Reviews

Pests in the City: Flies, Bedbugs, Cockroaches, and Rats by Dawn Day Biehler. 2013. Weyehaeuser Environmental Books. University of Washington Press. Seattle, Washington, USA. 338 pp. ISBN: 0295993014 (hardbound, in English)

Charlotte Aldebron1

In the back office of a Washington D.C. museum, a full-grown female Homo sapiens plods along, dutifully preserving specimens. After a long winter of mindless work, her intellectual hunger is reaching its peak. This morning she senses that with the blossoming cherry trees, an equally delightful opportunity is about to bloom. Sure enough a book for review is handed to her and she hastily grabs at it, desperate eyes roaming the cover and its folds. She would have taken any book but this one looks to be a feast. A week later her mind is beyond sated. Her senses have changed. The city around her is no longer crawling with tourists but with survivors of a century long battle for pest management and social equality. With this newfound insight, the human being begins to spread the word.

Dawn Day Biehler’s “Pests in the City: Flies, Bedbugs, Cockroaches, and Rats” published by Weyehaeuser Environmental Books charts the relationship between humans and pests in U.S. cities from the end of the 19th century to the present day. The relationship is a tumultuous one that not only pits humans against nature but humans against humans and humans against themselves. Each chapter in part one begins from the point of view of a pest. These introductions are the most entomologically focused part of the book, leading the reader on the wings of a female fly as she travels from a horse manure pile to a baby’s bottle or taking us for a ride on the back of a hungry rat as it rummages in fallen garbage bins for scraps. Once we can understand the geography of an urban environment from the perspective of these beings, Biehler is quick to establish their place within human history, their introductions to the U.S., and their impact on human health. Where Biehler really spends her time, however, is on the role of pests as indicators of social inequality and as catalysts for improved desegregation, housing reform, and environmental justice. This is no tale of the horrors of the bubonic plague, swarms of locusts devastating crops, and rabies-ridden rodents. This is the tale of humans forced to live in squalor and faced with an onslaught of social stigmas. This is the story of the pest

1 Washington, District of Columbia, USA 20017. E-mail: [email protected]

DOI:10.9784/LEB2(1)Aldebron.01 Electronically available on May 16, 2014. Mailed on May 13, 2014. Life: The Excitement of Biology 2(1) 65

control industry withholding services in cities with government financed pest management, however poor the funding and reach, therefore making a pest-free existence a luxury only the affluent, often whites, could enjoy. This is an odyssey of the disenfranchised, struggling to maintain sovereignty over their homes and finding power in numbers, as communities banded together. Pests are the vectors of physical disease just as they are the vectors of social disease, Biehler asserts. But while medical advances have brought us temporary relief from the physical ailments that flies, bedbugs, cockroaches, and rats bring, we have yet to make the social advances necessary to eliminate the conditions in which these beings continue to thrive, constant reminders of the emotional, financial, and physical distress that burdens the lower classes, a majority of whom are minorities. Biehler’s thoroughness is unabashed. Even before part two, the reader is well acquainted with three principle dichotomies present in the fight for a pest free existence. These are: 1) On the one hand, those living with pests were seen and portrayed as incubators of disease. These populations, however, were comprised primarily of poor immigrants and blacks who, once they made it into cities, were forced to inhabit neighborhoods that were abandoned by Anglos, houses already falling into disrepair, infrastructures already crumbling, landlords unwilling to schedule consistent trash collection or outhouse maintenance. All of those conditions are conducive to the harboring of pests. 2) There is a wavering line between public and private responsibility of pest management. In the private domain, women bear the burden of fortifying their homes. Pests, however, do not abide by the borders between houses or apartments or even neighborhoods. Making pests a community concern and therefore worthy of public funding is fundamental, though residents are wary of admitting they have infestations because of the associated social stigma and likelihood of being denied housing. And 3) The modernization of pest-control methods brought forth both hope and unforeseen consequences. Pesticides once seemed like cure-alls even though they masked the unjust social conditions under which pests thrived. But chemical methods also put humans at risk of poisoning, wreaked havoc with ecosystems as they bled into other facets of the food webs, and actually changed the genetic makeup of cockroach and rat populations as they adapted to pesticides, requiring even harsher concoctions. Though the city-focused case studies are extensive and the dimensions from which Dawn Day Biehler approaches this subject are countless, she does fall short is in any offerings of hope for the future. In fact, throughout the entire chronology of pest control, any optimism for true change is tempered by the reminder that even when the president of the United States of America emphatically declared the rat problem a race problem and allocated funds for a huge housing overhaul, a war in another country took precedent and hopeful inner-city residents were once again subjected to a bait-and-switch of fortunes. As readers, we are left adrift in a sea of approaches to integrated pest Life: The Excitement of Biology 2(1) 66

management that have not quite hit the mark and for all we know, never may. Biehler also glosses over the ways in which her cities of focus are dramatically changing in the 21st century. Washington D.C. is in the midst of massive gentrification in which many of the multi-generational black families are being priced out of their neighborhoods and into the suburbs. Young, upper-middle class whites are descending on blocks previously ravaged by poverty and now gleaming with brand-new condos. What does this change in demographics and geography mean for pest populations? Will the needs of minorities be met as they cross into bordering states and become “someone else’s problem”? Perhaps an even more startling omission is the populations of immigrants. While first generation Italians and Chinese are mentioned with respect to the crowding of blocks during the early 20th century, no mind is paid to the recent waves of Salvadorans, Mexicans, Puerto Ricans, Dominicans and Vietnamese who have to deal with language and immigration status barriers when it comes to broaching the subject of infestations within their tight living quarters. “Pests in the City,” uses city specific vermin to highlight the more destructive problems of racism and environmental degradation in the 20th century. These pests are unavoidable evidence of human ignorance and, more powerfully, symbols of our own resilience in the face of adversity. Perhaps in embracing the latter rather than emphasizing the former, we can finally progress.

Life: The Excitement of Biology 2(1) 67

Book Reviews

Jorge A. Santiago-Blay2

Britain’s Dragonflies. A field guide to the damselflies and dragonflies of Britain and Ireland (Third Edition. Fully revised and updated.) by Dave Smallshire and Andy Swash. 2014. WILDGuides Ltd. Princeton University Press. Princeton, New Jersey, USA. 224 pp. ISBN: 978-0-691-16123-5 (softbound, in English)

Yesterday, as I was driving 160 km to work, I was deliberating the layout of a new book a colleague of mine and I are planning. I want standardization so that the topic at hand is readily captured, with colors neatly ascribed to certain ideas. Just like the Meditations book (see below), Britain’s Dragonflies gave me exactly what the proverbial doctor recommended: an example of a well- designed book. Thanks to Smallshire and Swash, readers get a concert by these rock-and-roll, high energy, and aerial predators (p. 7). After the gloriously illustrated sections on the biology and the ecology of British and Irish native odonatans, 20 species of damselflies and 26 of dragonflies (plus 15 confirmed or potential vagrants, two former breeders, p. 152, as well as introduced species, p. 188) are discussed using a consistent concise yet wildly informative template (p. 59). These species summaries include, among others, scientific name, common name (in English), a scale bar, conservation status and legislation, distribution (in time and space), adult identification, behavior, breeding habitats, remarks on conservation, look-alikes, and the all-important color illustrations. The art work is gorgeous. The book concludes with sections on immature forms, also beautifully illustrated, additional comments on the conservation status of local odonatans, and an index. This tome, which is written in a reasonable legible font, should be of great help to anyone passionate about dragonflies and damselflies.

☼

Meditations with Thomas Berry, with additional material by Brian Swimme Selected by June Raymond. 2010. Green Spirit. London, England, United Kingdom. 110 pp. ISBN: 978-0-0552157-4-2 (softbound, in English)

Upon my arrival at work, I discovered that a kind person had placed a gift, Meditations, in my mailbox. Inside the book, a little message, “…Berry was a theologian, ecologist and philosopher. His thoughts can be interpreted on many levels. May you be able to take a few minutes here and there to ponder.” I could

2 217 Wynwood Road, York, Pennsylvania 17402 USA. E-mail: [email protected] Life: The Excitement of Biology 2(1) 68

not help but read the book in one sitting. Having just completed teaching an upper division ecology course, I lamented not having read it earlier in order to share some passages with my students. Although not a scientific book, Meditations certainly offers encouragement for our motivations, not only at the personal level but also all the way to the biospheric level. The book is divided into seven sections, each with generally a dozen or so short, nameless poems. A common theme in the section entitled, Creation’s Beauty and Violence, is the coexistence of stark contrasts (“the story of the universe is … a drama filled with both elegance and ruin”. I found the section, Diversity, hopeful because in view of such diverging phenomena, difficulties often ensue. Like a dear friend of mine likes to say, “when the going gets tough, the tough get going” or as Meditations puts it, “Only by dealing with the difficulty, does the creativity come forth.” (p. 25). This section also reminds us that “nature abhors uniformity” (p. 33) In the section Human Destruction, the following lines in particular resonated with me, stating in twelve words, a basic principle of biological interactions, “The universe is a community of subjects, not a collection of objects”.. The third, fourth and fifth sections, Interiority, Community and To be human, respectively, emphasize the genetic and environmental interconnectivity of all beings, including that of our miniscule companions on this little spec we call earth: http://movies.nationalgeographic.com/movies/mysteries-of-the-unseen-world/ , http://www.ted.com/talks/louie_schwartzberg_hidden_miracles_of_the_natural_ world . The seventh and last section, A new vision, contains this “novel” idea: “Our responsibility to the Earth is not simply to preserve it, it is to be present to the Earth in its next sequence of transformations.” (p. 102). I believe that my non-science major students in the Fall 2014 will get to hear, and I hope listen with attentiveness, to some of the jewels in Meditations.