Skip to content

Advertisement

  • Correspondence
  • Open Access

Quantifying the unquantifiable: why Hymenoptera, not Coleoptera, is the most speciose animal order

  • 1Email author,
  • 1,
  • 1,
  • 1 and
  • 1
BMC Ecology201818:21

https://doi.org/10.1186/s12898-018-0176-x

  • Received: 24 March 2018
  • Accepted: 13 June 2018
  • Published:

Abstract

Background

We challenge the oft-repeated claim that the beetles (Coleoptera) are the most species-rich order of animals. Instead, we assert that another order of insects, the Hymenoptera, is more speciose, due in large part to the massively diverse but relatively poorly known parasitoid wasps. The idea that the beetles have more species than other orders is primarily based on their respective collection histories and the relative availability of taxonomic resources, which both disfavor parasitoid wasps. Though it is unreasonable to directly compare numbers of described species in each order, the ecology of parasitic wasps—specifically, their intimate interactions with their hosts—allows for estimation of relative richness.

Results

We present a simple logical model that shows how the specialization of many parasitic wasps on their hosts suggests few scenarios in which there would be more beetle species than parasitic wasp species. We couple this model with an accounting of what we call the “genus-specific parasitoid–host ratio” from four well-studied genera of insect hosts, a metric by which to generate extremely conservative estimates of the average number of parasitic wasp species attacking a given beetle or other insect host species.

Conclusions

Synthesis of our model with data from real host systems suggests that the Hymenoptera may have 2.5–3.2× more species than the Coleoptera. While there are more described species of beetles than all other animals, the Hymenoptera are almost certainly the larger order.

Keywords

  • Beetles
  • Inordinate fondness
  • Animal diversity
  • Parasitic wasps
  • Parasitoids
  • Species richness

“…if the micro-hymenopterists would get off their lazy asses and start describing species, there would be more micro-Hymenoptera than there are Coleoptera.”

Terry Erwin (in [1])

Background

The beetles (order Coleoptera), have historically [2, 3] and more recently [47] been described as the most speciose order of animals on Earth. The great diversity of beetles was sufficiently established by the middle of last century such that Haldane (possibly apocryphally)1 quipped that an intelligent creator of life must have had “…an inordinate fondness for beetles” [8]. However, what evidence underlies the claim that the Coleoptera are more species-rich than the other insect orders? Certainly, more species of beetles (> 350,000) have been described than any other order of animal, insect or otherwise [11, 12], but does this reflect their actual diversity relative to other insects? Though this may seem purely an academic question, its resolution informs our understanding of patterns and mechanisms of insect evolution (e.g., [1315]) and, to the extent that species richness is a proxy for ecological import [16, 17], how conservation efforts might best be directed.

Why are beetles thought to be so diverse in the first place? In part, historical biases in beetle collecting and an associated accumulation of taxonomic resources for the Coleoptera may have had an outsized influence on our perception of diversity. In the mid-to-late 1800s, beetles were prized among insects for their collectability. Many gentlemen of leisure—including, notably, Charles Darwin—collected beetles for sport and would make a great show of comparing the sizes of their respective collections [18, 19]. This preconception was then reinforced by studies that extrapolated from specific, targeted collections of insect diversity that focused on beetles. Of these, perhaps the highest in profile was a study conducted by Terry Erwin. Erwin [20] used an insecticide to fog the canopies of 19 individual Luehea seemannii trees in a Panamanian rainforest and then collected and identified the insect species that fell out of those trees. After having identified the proportion of the beetle species that were apparently host-specific to L. seemannii (163 of 955), he estimated that there might be as many as 12.2 million beetle species in the tropics. Similar studies seeking to estimate global insect diversity have also tended to emphasize beetles (e.g., [21, 22]).

Nevertheless, some previous work has challenged the canon, with various authors suggesting—though never quite insisting—that the Hymenoptera may be more speciose than the Coleoptera [2326]. The premise behind this suggestion is that most of the larvae of the Parasitica (one of the two infraorders of apocritan Hymenoptera; the other is the Aculeata, which includes ants, bees, and stinging wasps), are obligate parasites of insect and other arthropod hosts that feed on the host’s tissue until the host dies (≈ “parasitoids”). Why is this parasitic life history relevant to the Hymenoptera’s proportional contribution to insect diversity? Simply put, species of parasitoid Hymenoptera (including the Parasitica, as well as some other groups such as the Orussidae and some Chrysidoidea) attack all orders of insects as well as some non-insect arthropods [2729], and, reciprocally, most holometabolous insect species are attacked by at least one—and often many more than one—species of hymenopteran parasitoid [30, 31]. For instance, Hawkins and Lawton [32] examined parasitoid communities associated with 158 genera of British insects across five different orders, and found that parasitoid species richness ranged from 2.64 to 9.40 per host species across different host insect orders.

If parasitoid wasps are ubiquitous and most hosts are attacked by many different species, why is there any debate at all about the Hymenoptera being more diverse than other orders? One reason may be that estimates of the regional and global species-richness of parasitoid wasps remain elusive. Their small size and a relative paucity of taxonomic resources have left the parasitoid Hymenoptera relatively under-described compared to other insect orders [25, 33]. As a consequence, when collection-based estimates of regional insect diversity have been attempted, they have often excluded all but the largest and easiest-to identify families of parasitic Hymenoptera (e.g., [3436]; though see [37, 38]).

A second reason for uncertainty regarding the species richness of the parasitoid Hymenoptera is that their host ranges are often unknown. While it may be true that most insects harbor many parasitoid species, the question remains whether these parasitoid communities are exclusively composed of oligophagous or polyphagous wasps that attack many hosts, or if instead the average insect host tends to have some number of specialist wasps among its many predators (Fig. 1). Only in the latter case would one be able to confidently assert that the Hymenoptera is the largest of the insect orders.
Fig. 1
Fig. 1

An illustration of how uncertainty about specialist vs. generalist behaviours might lead to misleading conclusions about parasitoid species richness. In a, each host species (differently colored beetles) is attacked by two parasitoids. However, because all parasitoids attack all four beetles the overall species richness of hosts exceeds that of the parasitoids (i.e., P:H < 1). In b, while some hosts have only one parasitoid, overall parasitoid richness exceeds host richness (P:H > 1) because some parasitoids are more specialized

How then to approach this question without asking the micro-hymenopterists (and the coleopterists, dipterists, lepidopterists, etc.) to hurry up and describe all of the world’s insect species? We suggest two complementary approaches: (1) mathematically describing the values of parasitoid-to-host (“P:H”) ratios that would support—or contradict—the notion that the Hymenoptera is the most speciose insect order and (2) tabulating—wherever possible—actual P:H ratios for various genera of host insects.

What parasitoid-to-host ratios would suggest that the Hymenoptera are more species-rich than other insect orders?

For the Hymenoptera to be the largest order of insects, the global ratio of wasp parasitoids to hosts (P:H) need not—in fact—equal or exceed 1.0. Indeed, a global P:H of 1.0 (i.e., an average of one unique hymenopteran parasitoid species for each other insect species) would mean that parasitoids account for a full half of all insects. Instead, P:H ratios need only reach values such that the Hymenoptera are more species-rich than the next largest order (which, for the sake of argument, we will assume is the Coleoptera). Here, we work towards finding parameters that describe that space. First, it will be true that:
$$I\, = \,1\, - \,\left( {P\, + \,C} \right)$$
(1)
where P is the proportion of all insect species that are parasitoid Hymenoptera, C is the proportion of insects that are Coleoptera, and I is the remaining proportion of insect species, including the non-parasitoid Hymenoptera (Fig. 2a). Note that for the sake of simplicity we entirely exclude the many Hymenoptera that are parasitic on other parasitoids (“hyperparasitoids”).
Fig. 2
Fig. 2

Representations of the space where the number of parasitoid wasp species would outnumber the Coleoptera, given different parasitoid-to-host ratios for coleopteran hosts and for other insect hosts. a Pictorial representation of the model, wherein the total number of parasitoid species (P) will be the sum of the number of species of Coleoptera (C) and of other insects (I), each first multiplied by their respective overall parasitoid-to-host ratio (\(p_{C}\) or \(p_{I}\)); b black lines show results of the model for four different values of \(p_{I}\) and with \(p_{C}\) held at zero (i.e., when the average coleopteran has no specialist parasitoids). Where black lines overlap with gray shaded areas represents space where P > C; c results of four different scenarios in which \(p_{C}\) and \(p_{I}\) are equal; d some additional combinations of \(p_{C}\) and \(p_{I}\). Though both axes could continue to 1.0, some high values of P and C are not mathematically possible or biologically likely, and at P or C values above 0.5 the question about relative species-richness becomes moot

Additionally, because of the intimate relationship between parasitoids and their hosts, we can describe the proportion of species that are parasitoid Hymenoptera using the following expression:
$$P\, = \,C\left( {p_{C} } \right)\, + \,I\left( {p_{I} } \right),$$
(2)
where \(p_{C}\) and \(p_{I}\) represent the mean P:H ratios for all coleopterans and all non-coleopterans, respectively. The true values of \(p_{C}\) and \(p_{I}\) are unknowable, but can be estimated (see next section), and their use in this way allows for exploration of the ranges of P:H ratios that would result in different relative numbers of Hymenoptera and Coleoptera. Equation 2 again excludes hyperparasitoids, as well as parasitoids of non-insect arthropods, which makes P a conservative estimate of the proportion of insect species that are parasitoids.
Given these two relationships, we can substitute Eq. 1 into Eq. 2:
$$P\, = \,C\left( {p_{C} } \right)\, + \,p_{I} \, - \,p_{I} \left( {P\, + \,C} \right).$$
(3)

Equation 3 allows us to find the values of \(p_{C}\) and \(p_{I}\) that result in a P > C or vice versa. As shown in Fig. 2, the space where P > C includes a substantial area where \(p_{C}\) or \(p_{I}\) (or both) can be < 1. For instance, if the Coleoptera make up 25% of all insects, as suggested by many contemporary authors [22, 39], a \(p_{C}\) of only 0.25 (or one species-specialist parasitoid for every four beetle species), coupled with a \(p_{I}\) of 0.50, results in P = C (and the many tens of thousands of non-parasitoid Hymenoptera will then tip the scale in their favor). Even if the Coleoptera amount to 40% of the insects, which reflects the percentage of currently-described insect species that are beetles, there will be more parasitoid Hymenoptera than beetles if \(p_{C}\) and \(p_{I}\) are equal to or in excess of 0.67 (two specialist parasitoid species for every three host species).

Another way to explore the values of \(p_{C}\) and \(p_{I}\) at which P will be greater than C is to find the circumstances when the two will be equal. If we substitute C for P into Eq. 3, we get:
$$p_{C} \, = \,1\, + \,2p_{I} \, - \,\frac{{p_{I} }}{C}$$
(4)
We can then plot \(p_{C}\) vs \(p_{I}\) for values of C between 0 and 0.5 (Fig. 3). Here, each line represents circumstances when P = C, such that the area above and to the right of each line represents values of \(p_{C}\) and \(p_{I}\) that result in a P > C. Here again, \(p_{C}\) and \(p_{I}\) need not be particularly large for the parasitoid Hymenoptera to exceed the species richness of the Coleoptera. For instance, if one quarter of all insects are beetles, \(p_{C}\) and \(p_{I}\) need only exceed 0.4 (the equivalent of two parasitoid species for every five host species).
Fig. 3
Fig. 3

Plot based on Eq. 4, with five representations of circumstances when C and P are equal proportions (solid black lines). \(p_{I}\) = overall P:H ratio for non-coleopteran insect hosts; \(p_{C}\) = overall P:H ratio for the Coleoptera. Space above and to the right of each line represents values of \(p_{C}\) and \(p_{I}\) where P > C, while space below and to the left of each line represents values where C > P

What do actual P:H ratios look like in nature?

The next question becomes: can we estimate parasitoid: host ratios (e.g., \(p_{C} , \;p_{I}\)) for different host insects? Quantifying global P:H ratios for entire insect orders is as unapproachable as the task of counting all of the living insect species: not only are most Hymenoptera undescribed, host records for described species are often incomplete, such that multiplying each host species by its supposed number of specialist parasitoids may often inadvertently include parasitoids that share hosts (Fig. 4). While this is problematic, recognition of the problem helps present paths forward. For indeed, some host–parasitoid systems are exceedingly well studied and well-understood, such that we can be reasonably confident about the completeness of the host records of at least some parasitoids. With this information, we can calculate a metric that we call the genus-specialist parasitoid:host ratio. This metric interrogates all members of a host insect genus in the same geographic region and identifies all of the parasitoids known to attack only members of that genus (the “genus-specialist” parasitoids). Because this P:H ratio ignores all parasitoids known to attack any extra-generic host—as well as those whose host range is unknown or has been incompletely studied—it is therefore an extremely conservative estimate of the overall P:H ratio for an insect genus.
Fig. 4
Fig. 4

Known genus-specialist parasitoids can be used to calculate a minimum P:H ratio for an insect host genus. The focal beetle genus H (three species) has four known parasitoids, P1–P4. P1 and P4 are relatively well-studied, and known to be genus-specialists, attacking only hosts in this beetle genus. P3 has some known extra-generic hosts, while the host range of P2 is poorly studied and unknown extra-generic hosts may exist. For the purposes of estimating a genus-specialist P:H, one would therefore use only P1 and P4, such that a minimum P:H for this beetle genus would be 2/3, or 0.67. Note that if the total number and identities of extra-generic hosts were known for P2 and P3, a “true” P:H for the genus could be calculated (see “Synthesis”)

Below, we present four case studies, representing host–parasitoid systems with records sufficiently complete to allow for calculation of genus-specialist parasitoid:host ratios. For each system, we focus on a single host genus in North America. We restricted geography so that parasitoid numbers would not be inflated by large biogeographic differences between hosts in their parasitoid assemblages. North America was chosen because sampling is relatively strong, and several robust resources exist for Nearctic parasitoids (e.g., [29, 40, 41]).

For each system, we searched for all literature that mentioned the name of the host genus (or historical synonyms) and either “parasite” or “parasitoid” and compiled a database of records, performing reticulated searches on each parasitoid species name as it was added to the database in order to determine known parasitoids host ranges. From among all parasitoid records, we classified parasitoids as “genus-specialists” if they had only ever been reared from hosts in this same genus. We then split these “genus-specialists” into two groups: those for which an argument can be made that they do not have unknown extra-generic hosts, and those that were “possible genus-specialists” but for which records were less complete. Non-hymenopteran parasitoids (e.g., Tachinidae) were excluded, but in any case were only present for two of the four hosts we examined (Malacosoma and Neodiprion), and generally do not have the taxonomically cosmopolitan host ranges of the hymenopteran parasitoids. For cases where host genera were found on multiple continents, only host species in North America were included in the study, and to be conservative, a parasitoid was still considered “generalist” if it occurred on an extra-generic host species outside of North America. Introduced host species were noted but not counted in host lists, as they do not represent long-term host–parasite relationships. Introduced parasitoid species were included in generalist lists, regardless of whether they were specialists on that genus in North America or elsewhere. We describe each system below and refer the reader to additional materials for species lists, specialist/generalist classifications, and citations. A summary of data across the four genera and references for these data can be found in Additional files 1 and 2.

System 1: Rhagoletis (Diptera: Tephritidae)

Many North American Rhagoletis flies are pests of agriculturally-important fruits. Eggs are deposited in ripening fruits by the female fly, and larvae develop through several instars while feeding on fruit pulp [42]. For most species, larvae then exit the fruit and pupate in the soil. Parasitoids are known from egg, larval and pupal stages of many Rhagoletis species. Several studies have described the parasitoid communities associated with Rhagoletis agricultural pest species (e.g., [4246]), though records of parasitoids of non-pest species also exist (e.g., [4749]). Moreover, many of the associated parasitoid species are well-studied in their own right, with robust records of their biology, ecology, and host-ranges [45, 5052].

Of the 24 species of North American Rhagoletis flies, 16 have a published record of parasitoid associations. Across these 16 flies, we found records of 39 parasitoid species, among which 24 “genus-specialists” have been described only from North American Rhagoletis and no other insect host (Additional file 1: Table S1). Of these, we set aside three “possible” genus-specialist species that did not have a strong collection record and for which host records may possibly be incomplete. The remaining set of genus-specialists included 14 braconids (genera Diachasma, Diachasmimorpha, Utetes, and Opius), six diapriids (genus Coptera), and a pteromalid (genus Halticoptera). The genus-specialist P:H ratio for Rhagoletis is therefore either 1.31 (21/16), or 1.50 (24/16), depending on whether “possible genus-specialists” are included. An extra-conservative P:H ratio might also include the eight Rhagoletis hosts that have no record of parasitoids (P:H = 21/24 = 0.88), though this almost certainly ignores some number of unknown genus-specialist parasitoids.

Some of the 15 “generalist” parasitoids of Rhagoletis have been reared from a diverse set of extra-generic hosts, but in some cases only from one other fruit-infesting tephritid (e.g., Phygadeuon epochrae and Coptera evansi, both of which have only been reared from Rhagoletis and from Epochra canadensis [Diptera: Tephritidae]). These 15 “generalists” are listed in Additional file 1: Table S1.

System 2: Malacosoma (Lepidoptera: Lasiocampidae)

The tent caterpillars (genus Malacosoma) are shelter building, cooperatively-foraging moths that damage both coniferous and deciduous trees across at least 10 families. Most species use > 1 host tree genus, though some (e.g., Malacosoma constrictum; Malacosoma tigris) are more specialized [53]. There are six North American species of Malacosoma, some with overlapping geographic distributions [53]. Female moths lay eggs in a mass wrapped around a branch of the host tree. Larvae of most species (M. disstria is an exception) live colonially inside “tents” made of spun silk and make regular excursions to feed on host leaves. The caterpillar stage is eaten by birds, mammals and several insect predators, but the most taxonomically diverse natural enemies are the parasitoids [53]. Of these, approximately one-third are Dipteran (family Tachinidae), while the remaining two-thirds are Hymenopteran parasitoids. Parasitoids attack all immature life stages, but most appear to emerge during the pre-pupal or pupal stage. Parasitoids of the North American tent caterpillars have been well documented, and often in the context of other available forest caterpillar hosts, such that it is reasonable to assert that some parasitoid species are Malacosoma-specific (e.g., [5456]).

All six of the North American Malacosoma species have at least one known parasitoid association, and we compiled a total of 78 different parasitoid species across all hosts (Additional file 1: Table S2). Of these, eleven had only been reared from Malacosoma. Five of these eleven species we assigned to the “possible genus-specialists” category, as they had not been assigned a specific name (which makes it hard to determine whether other hosts exist), or because they had only been reared a single time from the host. The remaining six “genus-specialists,” were from four different hymenopteran families. The genus-specialist P:H ratio for Malacosoma is therefore between 1.00 and 1.83.

Malacosoma have many more “generalists” than Rhagoletis: 68 species have been reared from both Malacosoma and at least one other extra-genetic host (Additional file 1: Table S2). Many of these appear to be specific to Lepidopteran hosts.

System 3: Dendroctonus (Coleoptera: Curculionidae)

Approximately 14 species of Dendroctonus bark beetles are found in North America [57]. Dendroctonus are specific to conifers in family Pinaceae, and can be highly destructive to their host trees. Female beetles construct nuptial chambers in trees where they mate with males and then deposit eggs in tunnels in the phloem. Larvae feed on phloem and outer bark and leave the tree only after pupation and adult emergence [57]. Most species are tree genus- or species-specific.

Parasitoids have been described for eight of the 14 North American Dendroctonus species, though for two of these (D. adjunctus and D. murryanae) only one or two parasitoid species are known. The total list of Dendroctonus-associated parasitoids is long, but the records are also often problematic, as Dendroctonus share their habitat with several other genera of bark beetles, which may or may not be attacked by the same parasitoids. In many studies, parasitoids are listed as “associates” of either Dendroctonus, or of one of the other species, or of both, but this does not always necessarily mean that a parasitoid attacks that beetle [5860]. We have here again tried to be conservative, though in one case (Meterorus hypophloei) we have ignored a claim of “association” with Ips beetles [61] as it did not seem to be well justified and other authors describe M. hypophloei as a Dendroctonus frontalis specialist [60, 62]. In total, we found nine Dendroctonus genus-specialists, two possible genus-specialists, and 48 “generalists” (Additional file 1: Table S3). The genus-specific P:H ratio for Dendroctonus is therefore between 1.13 and 1.38.

System 4: Neodiprion (Hyemenoptera: Diprionidae)

Neodiprion is a Holarctic genus of pine-feeding sawflies specializing on conifers in the family Pinaceae [63]. These sawflies have close, life-long associations with their tree hosts. The short-lived, non-feeding adults mate on the host plant shortly after eclosion, after which the females deposit their eggs into pockets cut within the host needles. The larvae hatch and feed externally on the host needles throughout development, and then spin cocoons on or directly beneath the host [6466]. Many species also have highly specialized feeding habits, and feed on a single or small handful of host-plant species in the genus Pinus. Since many of the ~ 33 Neodiprion species native to North America are considered economic pests [67], considerable effort has gone into describing their natural history and exploring potential methods to control Neodiprion outbreaks.

Despite the wealth of natural history information, compiling a list of parasitoids attacking Neodiprion is complicated by a history of accidental and intentional introductions. In addition to the native species, the European pine sawfly, Neodiprion sertifer, and three species from the closely related genera Diprion and Gilpinia were introduced in the past ~ 150 years and have spread across the United States and Canada [6871]. In an attempt to control these invasive pests, several parasitoids have been introduced, and now attack both native and invasive diprionids [7274].

We found 20 genus-specialist parasitoid species associated with the 21 species of North American Neodiprion for which parasitoid records exist. An additional seven parasitoids were classified as “possible” genus-specialists. The genus-specific P:H ratio for Neodiprion is therefore between 0.95 and 1.29. An additional 51 species had been reared from both Neodiprion and an extra-generic host, with nine introduced parasitoids. We also compiled a list of 14 introduced parasitoids, nine hyperparasitoids, and 28 tachinid (Diptera) parasitoids of Neodiprion (Additional file 1: Table S4), but these were not included in any analyses.

Synthesis

Upon considering our model together with actual estimates of P:H ratios from natural host systems (Table 1), there appear to be few conditions under which the Hymenoptera would not be the largest order of insects. If, for instance, the P:H ratios for Rhagoletis, Malacosoma, Dendroctonus, and Neodiprion are at all representative of other hosts in those respective orders, and we use them to calculate relative species richness based on recent counts of only the described species in each order [75], the Hymenoptera exceed the Coleoptera by 2.5–3.2 times (Table 2). Recall that these calculations ignore all hyperparasitoids, and also omit parasitoids of other insect orders (e.g., Hemiptera, Orthoptera) and of non-insect arthropods. Even if we use half of the lowest P:H ratio estimate for each of the four largest orders, the Hymenoptera would outnumber the Coleoptera by more than 1.3 times.
Table 1

Summary of estimates of parasitoid to host (P:H) ratios for four host insect genera

Focal host genus

# NAm species (# with parasitoid records)

P:H (overall)

P:H (genus-specialists only)

P:H (specialist) [including possible genus-specialists]

Genus-specialist families

Rhagoletis (Diptera: Tephritidae)

24 (16)

2.44

1.31

1.50

Braconidae; Diapriidae; Pteromalidae

Malacosoma (Lepidoptera: Lasiocampidae)

6 (6)

13.00

1.00

1.83

Braconidae; Eulophidae; Ichneumonidae; Platygastridae

Dendroctonus (Coleoptera: Curculionidae)

14 (8)

6.50

1.13

1.38

Braconidae; Ichneumonidae; Gasteruptiidae; Proctotrupidae; Pteromalidae; Platygastridae

Neodiprion (Hymenoptera: Diprionidae)

33 (21)

3.48

0.95

1.29

Ichneumonidae; Chrysididae

Shown for each host genus are: the total number of North American (NAm) species, as well as the number with parasitoid records; the overall P:H, which includes generalist species; the genus-specialist P:H; and the genus-specialist P:H when “possible genus-specialists” were included. Parasitoid families that were among each group of genus-specialists are also listed

Table 2

Calculations of hymenopteran species richness, given numbers of described insect species in other orders and P:H ratios estimated in this paper

 

High P:H estimates from case studies

Low P:H estimates from case studies

Half of lowest estimates from case studies

Diptera (152,244)

228,366

199,440

99,720

Lepidoptera (156,793)

286,931

156,793

78,397

Coleoptera (359,891)

494,850

406,677

203,338

Non-parasitoid Hymenoptera (~ 62,000)

79,980

58,900

29,450

All other insect orders (335,970)

0a

0a

0a

Total parasitoid Hymenoptera

1,107,487

833,590

416,795

Non-parasitoid Hymenoptera (to add to calculated parasitoid numbers)

62,000

62,000

62,000

Total Hymenoptera

1,152,127

883,810

472,905

Combining conservative P:H ratio estimates from four case studies with numbers of described species in the four largest insect orders [33, 75] offers an idea of how species richness of the Hymenoptera may compare with that of other orders

aParastioids attack hosts in all other insect orders, but these are omitted as we did not estimate P:H ratios for any hosts in these orders. Total numbers therefore exclude large numbers of hymenopteran species

Note that P:H ratios might be measured more accurately and/or calculated in different ways, most of which we would expect to increase the estimates of P:H reported here. For instance, rather than ignoring all of the so-called “generalist” parasitoids, one could identify those for which host ranges are known (e.g., Fig. 4), divide each by the total number of host genera attacked, and add that fraction to the numerator of the P:H ratio for the focal host genus. As one example, the “generalist” parasitoids Phygadeuon epochrae and Coptera evansi both attack only Rhagoletis flies and the currant fly Epochra canadensis. These would each add an additional 0.5 to the other 24 “genus-specialist” parasitoids of Rhagoletis, giving a revised P:H of 1.56. For Malacosoma, Dendroctonus, and Neodiprion, which all have many “generalist” parasitoids with host ranges that include only a few other extra-generic hosts in the same respective family, such additions should increase P:H ratio estimates by a considerable margin.

Another way to calculate P:H would be to focus not on a host genus but on hosts sharing the same habitat. For instance, Dendroctonus bark beetles share their habitat niche with several other species of beetle, and many of their parasitoids are “specialists” in the sense that they attack more than one bark beetle, but all within the same tree habitat [60]. One could, therefore, calculate a P:H where H is the number of potential beetle host species in the habitat, and P is the number of “habitat-specialist” parasitoid species (those that attack one or more of the hosts in that habitat and no other hosts in other habitats).

Our analyses largely ignore the increasingly common finding that many apparently polyphagous insects—both herbivores and parasitoids—show evidence of additional host-associated genetic structure that might, if considered here as distinct lineages, change P:H ratios (e.g., [7681]). Indeed, all four of our focal host genera have named subspecies or show evidence for host-associated, reproductively-isolated lineages [57, 8284]. Though we chose to “lump” subspecies and other reproductively isolated lineages together for this analysis, it is interesting to consider how a detailed study of genetic diversity and reproductive isolation among a host genus and all of its associated parasitoids might change P:H ratios. Studies of the flies in the Rhagoletis pomonella species complex and three of their associated parasitoids suggest that where additional host-associated lineages are found in a phytophagous insect, this cryptic diversity may be multiplied many times over in its specialist parasitoid community [51, 85]. If broadly true, this implies that genus-specific P:H ratios may often be much higher than we report here.

One sensible criticism will surely be: to what extent are the P:H ratios for these four genera reflective of global P:H ratios for their respective orders (Coleoptera, Lepidoptera, Diptera, and the non-parasitoid Hymenoptera)? Surely some insect genera escape parasitism, and perhaps the examples chosen here simply have exceptionally large, or unusually specialized, parasitoid communities. As to the former, it may be that such escape artists exist, but they also may be relatively rare. After all, there are parasitoids that attack aquatic insects [86, 87], that parasitize insects in Arctic communities (e.g., [88]), and even those that dig down into soils to unearth and oviposit into pupae [50]. The list of potential hosts for parasitoids also extends to many non-insect arthropods [89, 90]. As to the four example genera being representative of overly large parasitoid communities, all of their “overall” P:H numbers (Table 1) are actually below the means found for their respective orders in an extensive study of parasitoid communities in Britain [32], suggesting that these communities are of average, or slightly below-average, size.

A second, equally sensible, criticism is that a sample size of four offers only a limited glimpse of genus-specialist P:H ratios, and that the same data should be collected from additional host insect genera. Having started out with a list of nearly 50 potential host genera and finding host–parasitoid records to be inadequate for all but four, we wholeheartedly agree. There is a great need to assemble datasets of the type presented here for additional hosts, including from insects using other feeding niches, from other insect orders, and from insects outside of North America, especially in tropical forests. In the future, perhaps a more comprehensive analysis of P:H ratios will be possible.

Concluding thoughts

While it may indeed be premature to claim that the Hymenoptera is the largest order of insects based solely on our data, many other studies offer support for the same conclusion. In fact, the preponderance of evidence suggests that the common wisdom about the Coleoptera being the most speciose is the more dubious claim. Studies of insect diversity that reduce taxonomic biases have found the Hymenoptera to be the most species-rich in both temperate [37] and tropical [38] forests, as well as in other habits (e.g., [91, 92]) and across the entirety of the British Isles [17]. In addition, a mass-barcoding study of Canadian insects found both Hymenoptera and Diptera were more diverse than Coleoptera [93]. After Hymenoptera, the Coleoptera may not even be the second most-speciose order; several recent inventories of species diversity suggest that the Diptera may hold that title [17, 94, 95]. Moreover, other historically-accepted ideas about diversity of parasitoid hymenopterans have recently been questioned, including the apparent myth that parasitoids are one of only a few groups whose diversity decreases towards the tropics [9698]. In any case, we hope this commentary results in a redoubled effort to understand and describe the ecology and natural histories of parasitoid wasps, including host ranges and cryptic host-associated diversity, such that estimates of P:H can be made for additional host genera. We also hope to see similar efforts in other animal groups that may harbor great diversity but for which far too little is known about host ranges, such as in some particularly speciose orders of mites and nematodes (e.g., [99, 100]. In other words, and to again quote Erwin [20], we hope that “…someone will challenge these figures with more data.”

Footnotes
1

Whether or not Haldane ever actually said it exactly in this way is unresolved [8, 9]. This phrase does not occur in any of Haldane’s writing, but he does write that “The Creator would appear as endowed with a passion for stars, on the one hand, and for beetles on the other” [10].

 

Declarations

Authors’ contributions

AAF conceived of the study. All authors helped formulate a framework for addressing the questions in the paper, developed the logical model, and collected and analyzed data from the four host genera. AAF and RKB wrote the manuscript. All authors read and approved the final manuscript.

Acknowledgements

We thank Isaac Winkler, Anna Ward, Eric Tvedte, Miles Zhang, Glen Hood, and Matt Yoder for their thoughtful discussions and comments on this manuscript. Peter Mayhew and two anonymous reviewers provided helpful suggestions for improving the manuscript, particularly with regard to future directions.

Competing interests

The authors declare that they have no competing interests.

Availability of data and materials

The datasets supporting the conclusions of this article are included within the article and its additional files.

Consent for publication

Not applicable.

Ethics approval and consent to participate

Not applicable.

Funding

Projects funded by the National Science Foundation to AAF (DEB 1145355 and 1542269) led directly to the discussions that motivated this study.

Publisher’s Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.

Authors’ Affiliations

(1)
Department of Biology, University of Iowa, 434 Biology Building, Iowa City, IA 52242, USA

References

  1. Rice ME, Terry L. Erwin: she had a black eye and in her arm she held a skunk. Zookeys. 2015;500:9–24.View ArticleGoogle Scholar
  2. Kirby W, Spence W. An introduction to entomology. London: Longman, Hurt, Rees, Orme, and Brown; 1818.View ArticleGoogle Scholar
  3. Hutchinson GE. Homage to Santa Rosalia or why are there so many kinds of animals? Am Nat. 1959;93:145–59.View ArticleGoogle Scholar
  4. Oberprieler RG, Marvaldi AE, Anderson RS. Weevils, weevils, weevils everywhere. Zootaxa. 2007;1668:491–520.Google Scholar
  5. McKenna D, Farrell BD. Beetles (Coleoptera). In: Hedges S, Kumar S, editors. The timetree of life. Oxford: Oxford University Press; 2009. p. 278–89.Google Scholar
  6. Zhang ZQ. Animal biodiversity: an introduction to higher-level classification and taxonomic richness. Zootaxa. 2011;12:7–12.Google Scholar
  7. Zhang S-Q, Che L-H, Li Y, Liang Dan, Pang H, Ślipiński A, et al. Evolutionary history of Coleoptera revealed by extensive sampling of genes and species. Nat Commun. 2018;9:205.View ArticlePubMedPubMed CentralGoogle Scholar
  8. Gould S. A special fondness for beetles. Nat Hist. 1993;102:4–8.Google Scholar
  9. Williamson M. Haldane’s special preference. Linn. 1992;8:12–5.Google Scholar
  10. Haldane J. What is life? The Layman’s view of nature. London: Lindsay Drummond; 1949.Google Scholar
  11. Farrell BD. “Inordinate fondness” explained: why are there so many beetles? Science. 1998;281:555–9.View ArticlePubMedGoogle Scholar
  12. Bouchard P, Grebennikov VV, Smith ABT, Douglas H. Biodiversity of Coleoptera. In: Foottit RG, Adler PH, editors. Insect biodiversity: science and society. Oxford: Wiley-Blackwell; 2009. p. 265–301.View ArticleGoogle Scholar
  13. Mayhew PJ. Shifts in hexapod diversification and what Haldane could have said. Proc Biol Sci. 2002;269:969–74.View ArticlePubMedPubMed CentralGoogle Scholar
  14. Wiens JJ, Lapoint RT, Whiteman NK. Herbivory increases diversification across insect clades. Nat Commun. 2015;6:8370.View ArticlePubMedPubMed CentralGoogle Scholar
  15. Ferns PN, Jervis MA. Ordinal species richness in insects-a preliminary study of the influence of morphology, life history, and ecology. Entomol Exp Appl. 2016;159:270–84.View ArticleGoogle Scholar
  16. May RM. How many species are there on Earth? Science. 1988;241:1441–9.View ArticlePubMedGoogle Scholar
  17. Shaw MR, Hochberg ME. The neglect of parasitic Hymenoptera in insect conservation strategies: the British fauna as a prime example. J Insect Conserv. 2001;5:253–63.View ArticleGoogle Scholar
  18. Browne J. Charles Darwin: voyaging. Princeton: Princeton University Press; 1996.Google Scholar
  19. Sheppard CA. Benjamin Dann Walsh: pioneer entomologist and proponent of Darwinian theory. Annu Rev Entomol. 2004;49:1–25.View ArticlePubMedGoogle Scholar
  20. Erwin TL. Tropical forests: their richness in Coleoptera and other arthropod species. Coleopt Bull. 1982;36:74–5.Google Scholar
  21. Ødegaard F. How many species of arthropods? Erwin’s estimate revised. Biol J Linn Soc. 2000;71:583–97.View ArticleGoogle Scholar
  22. Stork NE, McBroom J, Gely C, Hamilton AJ. New approaches narrow global species estimates for beetles, insects, and terrestrial arthropods. Proc Natl Acad Sci USA. 2015;112:7519–23.View ArticlePubMedGoogle Scholar
  23. LaSalle J. Parasitic Hymenoptera, biological control and biodiversity. In: LaSalle J, Gauld ID, editors. Hymenoptera and biodiversity. Wallingford: CAB International; 1993. p. 197–215.Google Scholar
  24. LaSalle J, Gauld ID. Hymenoptera: their diversity, and their impact on the diversity of other organisms. In: LaSalle J, Gauld ID, editors. Hymenoptera and biodiversity. Wallingford: CAB International; 1993. p. 1–26.Google Scholar
  25. Gaston KJ. Spatial patterns in the description and richness of the Hymenoptera. In: LaSalle J, Gauld ID, editors. Hymenoptera and biodiversity. Wallingford: CAB International; 1993. p. 277–93.Google Scholar
  26. Austin AD, Dowton M. Hymenoptera: evolution, biodiversity, and biological control. Clayton: CSIRO Publishing; 2000.Google Scholar
  27. Gibson GAP, Huber JT, Woolley JB. Annotated Keys to the Genera of Nearctic Chalcidoidea (Hymenoptera). Ottawa: NRC Research Press; 1997.Google Scholar
  28. Wharton R, Marsh P, Sharkey M. Manual of the New World genera of the family Braconidae (Hymenoptera). Spec Publ Int Soc Hymenopterists. 1997;1:1–439.Google Scholar
  29. Noyes J. Universal Chalcidoidea Database. 2017. http://www.nhm.ac.uk/chalcidoids. Accessed 21 Mar 2018.
  30. Schoenly K. The predators of insects. Ecol Entomol. 1990;15:333–45.View ArticleGoogle Scholar
  31. Memmott J, Godfray HCJ. Parasitoid webs. In: Lasalle J, Gauld ID, editors. Hymenoptera and biodiversity. Wallingford: CAB International; 1993. p. 217–34.Google Scholar
  32. Hawkins BA, Lawton JH. Species richness for parasitoids of British phytophagous insects. Nature. 1987;326:788–90.View ArticleGoogle Scholar
  33. Huber JT. Biodiversity of Hymenoptera. In: Foottit RG, Adler PH, editors. Insect biodiversity: science and society. Oxford: Wiley; 2009. p. 303–23.View ArticleGoogle Scholar
  34. Novotny V, Basset Y, Miller SE, Weiblen GD, Bremer B, Cizek L, et al. Low host specificity of herbivorous insects in a tropical forest. Nature. 2002;416:841–4.View ArticlePubMedGoogle Scholar
  35. Pietsch TW, Bogatov VV, Amaoka K, Zhuravlev YN, Barkalov VY, Gage S, et al. Biodiversity and biogeography of the islands of the Kuril Archipelago. J Biogeogr. 2003;30:1297–310.View ArticleGoogle Scholar
  36. Basset Y, Cizek L, Cuénoud P, Didham RK, Guilhaumon F, Missa O, et al. Arthropod diversity in a tropical forest. Science. 2012;338:1481–4.View ArticlePubMedGoogle Scholar
  37. Gaston KJ. The magnitude of global insect species richness. Conserv Biol. 1991;5:283–96.View ArticleGoogle Scholar
  38. Stork NE. The composition of the arthropod fauna of Bornean lowland rain forest trees. J Trop Ecol. 1991;7:161–80.View ArticleGoogle Scholar
  39. Hamilton AJ, Novotný V, Waters EK, Basset Y, Benke KK, Grimbacher PS, et al. Estimating global arthropod species richness: refining probabilistic models using probability bounds analysis. Oecologia. 2013;171:357–65.View ArticlePubMedGoogle Scholar
  40. Peck O. A catalogue of the Nearctic Chalcidoidea (Insecta: Hymenoptera). Mem Entomol Soc Canada. 1963;95:5–1092.View ArticleGoogle Scholar
  41. Krombein K, Hurd P, Smith D, Burks B. Catalog of Hymenoptera in America North of Mexico. Washington, D.C.: Smithsonian Institution Press; 1979.Google Scholar
  42. Bush GL. The taxonomy, cytology, and evolution of the genus Rhagoletis in North America (Diptera, Tephritidae). Bull Museum Comp Zool. 1966;134:431–562.Google Scholar
  43. Lathrop F, Newton R. The biology of Opuis melleus Gahan, a parasite of the blueberry maggot. J Agric Res. 1933;46:143–60.Google Scholar
  44. Cameron P, Morrison F. Psilus sp. (Hymenoptera: Diapriidae), a parasite of the pupal stage of the apple maggot, Rhagoletis pomonella (Diptera: Tephritidae) in south-western Quebec. Phytoprotection. 1974;55:13–6.Google Scholar
  45. Wharton RA, Marsh PM. New World Opiinae (Hymenoptera: Braconidae) parasitic on Tephritidae (Diptera). J Washingt Acad Sci. 1978;68:147–67.Google Scholar
  46. Feder JL. The effects of parasitoids on sympatric host races of Rhagoletis pomonella (Diptera: Tephritidae). Ecology. 1995;76:801–13.View ArticleGoogle Scholar
  47. Rull J, Wharton R, Feder JL, Guillén L, Sivinski J, Forbes A, et al. Latitudinal variation in parasitoid guild composition and parasitism rates of North American hawthorn infesting Rhagoletis. Environ Entomol. 2009;38:588–99.View ArticlePubMedGoogle Scholar
  48. Forbes AA, Hood GR, Feder JL. Geographic and ecological overlap of parasitoid wasps associated with the Rhagoletis pomonella (Diptera: Tephritidae) species complex. Ann Entomol Soc Am. 2010;103:908–15.View ArticleGoogle Scholar
  49. Forbes AA, Satar S, Hamerlinck G, Nelson AE, Smith JJ. DNA barcodes and targeted sampling methods identify a new species and cryptic patterns of host specialization among North American Coptera (Hymenoptera: Diapriidae). Ann Entomol Soc Am. 2012;105:608–12.View ArticleGoogle Scholar
  50. Muesebeck C. The Nearctic parasitic wasps of the genera Psilus Panzer and Coptera Say (Hymenoptera, Proctotrupoidea, Diapriidae). Technical Bulletin 1617. Washington, D.C.: United States Department of Agriculture Science and Education Administration; 1980.Google Scholar
  51. Forbes AA, Powell THQ, Stelinski LL, Smith JJ, Feder JL. Sequential sympatric speciation across tropic levels. Science. 2009;323:776–9.View ArticlePubMedGoogle Scholar
  52. Wharton R, Yoder M. Parasitoids of fruit-infesting Tephritidae. 2017. http://paroffit.org. Accessed 20 Mar 2018.
  53. Fitzgerald TD. The tent caterpillars. Ithaca: Cornell University Press; 1995.Google Scholar
  54. Langston RL. A synopsis of hymenopterous parasites of Malacosoma in California (Lepidoptera, Lasiocampidae). In: Lingsley E, Smith R, Steinhaus E, Usinger R, editors. University of California publications entomology, vol. 14. Berkeley: University of California Press; 1957. p. 1–50.Google Scholar
  55. Stacey L, Roe R, Williams K. Mortality of eggs and pharate larvae of the eastern tent caterpillar, Malacosoma americana (F.) (Lepidoptera: Lasiocampidae). J Kansas Entomol Soc. 1975;48:521–3.Google Scholar
  56. Shaw S. Aleiodes wasps of eastern forests: a guide to parasitoids and associated mummified caterpillars. FHTET-2006-08. Washington, D.C.: United States Department of Agriculture Forest Service, Forest Health Technology Enterprise Team; 2006.Google Scholar
  57. Six DL, Bracewell R. Dendroctonus. In: Vega FE, Hofstetter RW, editors. Bark beetles: biology and ecology of native and invasive species. Oxford: Academic Press; 2015. p. 305–50.View ArticleGoogle Scholar
  58. Overgaard N. Insects associated with southern pine beetle in Texas, Louisiana, and Mississippi. J Econ Entomol. 1968;61:1197–201.View ArticleGoogle Scholar
  59. Langor DW. Arthropods and nematodes co-occurring with the eastern larch beetle, Dendroctonus simplex [Col.: Scolytidae], in Newfoundland. Entomophaga. 1991;36:303–13.View ArticleGoogle Scholar
  60. Berisford CW. Parasitoids of the southern pine beetle. In: Coulson R, Klepzig K, editors. South Pine Beetle II General Tech Rep SRS-140. Asheville: United States Department of Agriculture Forest Service, Southern Research Station; 2011. p. 129–39.Google Scholar
  61. Kulhavy D, Goyer RA, Bing JW, Riley M. Ipps spp. natural enemy relationships in the Gulf Coastal states. Stephen F Austin State Univ Fac Publ. 1989;300:157–67.Google Scholar
  62. Stein CR, Coster JE. Distribution of some predators and parasites of southern pine beetle in two species of pine. Environ Entomol. 1977;6:689–94.View ArticleGoogle Scholar
  63. Smith DR. Systematics, life history, and distribution of sawflies. Sawfly life history adaptations to woody plants. San Diego: Academic Press; 1993. p. 3–32.Google Scholar
  64. Coppel HC, Benjamin DM. Bionomics of the nearctic pine-feeding Diprionids. Annu Rev Entomol. 1965;10:69–96.View ArticleGoogle Scholar
  65. Knerer G, Atwood CE. Diprionid sawflies: polymorphism and speciation. Science. 1973;179:1090–9.View ArticlePubMedGoogle Scholar
  66. Knerer G. Life history diversity in sawflies. In: Wagner MR, Raffa KF, editors. sawfly life history adaptations to woody plants. San Diego: Academic Press; 1993. p. 33–60.Google Scholar
  67. Arnett RH. American Insects: a handbook of the insects of America North of Mexico. Gainesville: Sandhill Crane Press; 1993.Google Scholar
  68. Britton W. A destructive pine sawfly introduced from Europe, Diprion (Lophyrus) simile Hartig. J Econ Entomol. 1915;8:379–82.View ArticleGoogle Scholar
  69. Gray D. Notes on the occurrence of Diprion frutetorum Fabr. in southern Ontario. Annu Rep Entomol Soc Ontario. 1938;68:50–1.Google Scholar
  70. Balch R. The outbreak of the European spruce sawfly in Canada and some important features of its bionomics. J Econ Entomol. 1939;32:412–8.View ArticleGoogle Scholar
  71. Schaffner JV Jr. Neodiprion sertifer (Geoff.), a pine sawfly accidentally introduced into New Jersey from Europe. J Econ Entomol. 1939;32:887–8.Google Scholar
  72. Finlayson LR, Reeks WA. Notes on the introduction of Diprion parasites to Canada. Can Entomol. 1936;68:160–6.View ArticleGoogle Scholar
  73. Finlayson T. Taxonomy of cocoons and puparia, and their contents, of Canadian parasites of some native Diprionidae (Hymenoptera). Can Entomol. 1963;95:475–507.View ArticleGoogle Scholar
  74. MacQuarrie CJK, Lyons DB, Lukas Seehausen M, Smith SM. A history of biological control in Canadian forests, 1882–2014. Can Entomol. 2016;148:S239–69.View ArticleGoogle Scholar
  75. Adler PH, Foottit R. Introduction. In: Foottit R, Adler P, editors. Insect biodiversity: science and society. Oxford: Wiley; 2009. p. 1–6.Google Scholar
  76. Drès M, Mallet J. Host races in plant-feeding insects and their importance in sympatric speciation. Philos Trans R Soc B Biol Sci. 2002;357:471–92.View ArticleGoogle Scholar
  77. Abrahamson WG, Blair CP, Eubanks MD, Morehead SA. Sequential radiation of unrelated organisms: the gall fly Eurosta solidaginis and the tumbling flower beetle Mordellistena convicta. J Evol Biol. 2003;16:781–9.View ArticlePubMedGoogle Scholar
  78. Stireman JO, Nason JD, Heard SB, Seehawer JM. Cascading host-associated genetic differentiation in parasitoids of phytophagous insects. Proc R Soc B Biol Sci. 2006;273:523–30.View ArticleGoogle Scholar
  79. Smith MA, Rodriguez JJ, Whitfield JB, Deans AR, Janzen DH, Hallwachs W, et al. Extreme diversity of tropical parasitoid wasps exposed by iterative integration of natural history, DNA barcoding, morphology, and collections. Proc Natl Acad Sci. 2008;105:12359–64.View ArticlePubMedGoogle Scholar
  80. Condon MA, Scheffer SJ, Lewis ML, Wharton R, Adams DC, Forbes AA. Lethal interactions between parasites and prey increase niche diversity in a tropical community. Science. 2014;343:1240–4.View ArticlePubMedGoogle Scholar
  81. Forbes AA, Devine SN, Hippee AC, Tvedte ES, Ward AKG, Widmayer HA, et al. Revisiting the particular role of host shifts in initiating insect speciation. Evolution. 2017;71:1126–37.View ArticlePubMedGoogle Scholar
  82. Stehr FW, Cook EF. A revision of the genus Malacosoma Hübner in North America (Lepidoptera: Lasiocampidae): systematics, biology, immatures, and parasites. Washington, D.C.: Smithsonian Institution Press; 1968.Google Scholar
  83. Powell THQ, Forbes AA, Hood GR, Feder JL. Ecological adaptation and reproductive isolation in sympatry: genetic and phenotypic evidence for native host races of Rhagoletis pomonella. Mol Ecol. 2014;23:688–704.View ArticlePubMedGoogle Scholar
  84. Bagley RK, Sousa VC, Niemiller ML, Linnen CR. History, geography and host use shape genomewide patterns of genetic variation in the redheaded pine sawfly (Neodiprion lecontei). Mol Ecol. 2017;26:1022–44.View ArticlePubMedGoogle Scholar
  85. Hood GR, Forbes AA, Powell THQ, Egan SP, Hamerlinck G, Smith JJ, et al. Sequential divergence and the multiplicative origin of community diversity. Proc Natl Acad Sci. 2015;112:E5980–9.View ArticlePubMedGoogle Scholar
  86. Juliano SA. Trichogramma spp. (Hymenoptera: Trichogrammatidae) as egg parasitoids of Sepedon fuscipennis (Diptera: Sciomyzidae) and other aquatic Diptera. Can Entomol. 1981;113:271–9.View ArticleGoogle Scholar
  87. Elliott JM. The life cycle and spatial distribution of the aquatic parasitoid Agriotypus armatus (Hymenoptera: Agriotypidae) and its caddis host Silo pallipes (Trichoptera: Goeridae). J Anim Ecol. 1982;51:923–41.View ArticleGoogle Scholar
  88. Fernandez-Triana J, Smith MA, Boudreault C, Goulet H, Hebert PDN, Smith AC, et al. A poorly known high-latitude parasitoid wasp community: unexpected diversity and dramatic changes through time. PLoS ONE. 2011;6:e23719.View ArticlePubMedPubMed CentralGoogle Scholar
  89. Lasalle J. North American genera of Tetrastichinae (Hymenoptera: Eulophidae). J Nat Hist. 1994;28:109–236.View ArticleGoogle Scholar
  90. Finch OD. The parasitoid complex and parasitoid-induced mortality of spiders (Araneae) in a Central European woodland. J Nat Hist. 2005;39:2339–54.Google Scholar
  91. Stahlhut JK, Fernández-Triana J, Adamowicz SJ, Buck M, Goulet H, Hebert PD, et al. DNA barcoding reveals diversity of Hymenoptera and the dominance of parasitoids in a sub-arctic environment. BMC Ecol. 2013;13:2.View ArticlePubMedPubMed CentralGoogle Scholar
  92. Kimsey L, Zavortink T, Kimsey R, Heydon S. Insect biodiversity of the Algodones Dunes of California. Biodivers Data J. 2017;5:e21715.View ArticleGoogle Scholar
  93. Hebert PDN, Ratnasingham S, Zakharov EV, Telfer AC, Levesque-Beaudin V, Milton MA, et al. Counting animal species with DNA barcodes: canadian insects. Philos Trans R Soc B Biol Sci. 2016;371:20150333.View ArticleGoogle Scholar
  94. Borkent A, Brown BV, Adler PH, de Amorim DS, Barber K, Bickel D, et al. Remarkable fly (Diptera) diversity in a patch of Costa Rican cloud forest: why inventory is a vital science. Zootaxa. 2018;4402:53–90.View ArticlePubMedGoogle Scholar
  95. Brown BV, Borkent A, Adler PH, de Amorim DS, Barber K, Bickel D, et al. Comprehensive inventory of true flies (Diptera) at a tropical site. Commun Biol. 2018;1:21.View ArticleGoogle Scholar
  96. Veijalainen A, Wahlberg N, Broad GR, Erwin TL, Longino JT, Saaksjarvi IE. Unprecedented ichneumonid parasitoid wasp diversity in tropical forests. Proc R Soc B Biol Sci. 2012;279:4694–8.View ArticleGoogle Scholar
  97. Eagalle T, Smith MA. Diversity of parasitoid and parasitic wasps across a latitudinal gradient: using public DNA records to work within a taxonomic impediment. FACETS. 2017;2:937–54.View ArticleGoogle Scholar
  98. Gómez IC, Sääksjärvi IE, Mayhew PJ, Pollet M, Rey del Castillo C, Nieves-Aldrey JL, et al. Variation in the species richness of parasitoid wasps (Ichneumonidae: Pimplinae and Rhyssinae) across sites on different continents. Insect Conserv Divers. 2017;11:305–16.View ArticleGoogle Scholar
  99. Grucmanová Ŝ, Holuša J. Nematodes associated with bark beetles, with focus on the genus Ips (Coleoptera: Scolytinae) in Central Europe. Acta Zool Bulg. 2013;65:547–56.Google Scholar
  100. Walter DE, Proctor HC. Mites: ecology, evolution & behaviour: life at a microscale. 2nd ed. Dordrecht: Springer; 2013.View ArticleGoogle Scholar

Copyright

© The Author(s) 2018

Advertisement