Composition of bodies of cave crickets (Hadenoecus subterraneus), their eggs, and their egg predator, Neaphaenops tellkampfi.
Adaptations to cave life may include reduction in pigmentation and vision, attenuation of appendages, production of fewer, larger offspring, reduced metabolic rates and prolonged life spans. Such features are most pronounced in obligate cave-dwelling troglobites (Barr, 1968; Culver, 1982). Trogloxenes, such as some bats, cave crickets and camel crickets, spend most of their time inside caves but leave to feed and are variably adapted to cave life.
Cave crickets, Hadenoecus subterraneus, have highly attenuated appendages (Studier and Lavoie, in press), produce fewer eggs per year than many other arthropods and show little seasonality in production of eggs (Cyr et al., 1991; but also see Kane and Poulson, 1976), have metabolic rates which are lower than predicted for similar size insects (Studier et al., 1986), are more susceptible than similar size insects to dehydration (Studier et al., 1987a) and exposures to temperatures exceeding average cave temperature are tolerated poorly (Studier and Lavoie, 1990). In their extensive study of taxonomic relationships and aspects of the biology of cave crickets, Hubbell and Norton (1978) suggested that H. subterraneus live ca. 9 mo as adults. Our ongoing mark-recapture study indicates that adults live at least 1.5 yr and our unfinished growth studies indicate that cave crickets require more than 1 yr to grow from hatching to maturity. Based on size frequency distributions and infrequent molting, T. Poulson (pers. comm.) suggests a minimal life span of 2-3 yr and a typical life span of 5 yr for H. subterraneus.
Our interests in aspects of nutrition of insectivorous bats and birds (Studier et al., 1988, 1991, 1994; Hungerford et al., 1993) prompted an earlier study of nitrogen and mineral composition of surface dwelling, especially flying, insects (Studier and Sevick, 1992). In view of extreme differences in anatomy, physiology, reproduction and reproductive cycles, growth rates and many other aspects of the biology of surface and cavernicolous insects, I expected that nitrogen and mineral concentrations in cave crickets, Hadenoecus subterraneus, might differ in comparison with epigean, especially other orthopteran, insects.
The predaceous, trechine cave beetle, Neaphaenops tellkampfi, is a troglobitic species that is a specialist on fertilized cave cricket eggs (Kane et al., 1975; Norton et al., 1975; Kane and Poulson, 1976). While ecological relationships between these species have been investigated (Griffith, 1992; Griffith and Poulson, 1993), nutritional studies have dealt only with energy budgets (Studier et al., 1986; Griffith and Poulson, 1993). Since insects often conform to the concept of "you are what you eat" (Slansky and Scriber, 1985; Dadd, 1985), nitrogen and mineral levels in bodies of these cave beetles were determined and compared to composition of both fertilized cave cricket eggs and epigean beetles.
MATERIALS AND METHODS
Adult and subadult cave crickets of a range of sizes were collected by hand from the walls and ceilings of Walnut Hill Cave, located ca. 2 miles by road from Park City, Kentucky, between 1000 and 1200 hr on 23 July 1994. Collected individuals were transported, in plastic bags containing wetted paper, in a styrofoam cooler to Maple Springs Research Station, Mammoth Cave National Park (MCNP), where they were frozen. Hind femur lengths (HFL) of thawed crickets were measured to the nearest 0.1 mm with calipers, crickets were dissected to remove all crop contents (which may be equal in mass to their remaining body), and wet crop-empty mass was determined (to 0.1 mg). These individuals were placed on small labelled pieces of aluminum foil and dried at 50-60 C at least 8 h in an ordinary oven.
On 24 July 1994, recently hatched, unfed, nonpigmented cave crickets ("whities") were collected by hand from the walls and ceiling within 20 m of the "Bubbly Pit" area of Great Onyx Cave, MCNP, Kentucky. Fertilized ova were also collected there on 24 July 1994 by hand after sifting potential egg-laying substrate through screen cloth. Finally, Neaphaenops tellkampfi, with visibly empty guts, were also collected at that site on 20 July 1994. To further ensure that their guts were quite empty (Studier et al., 1986), beetles were held at that collection site for 4 days in small, open, plastic test tubes whose walls were too high for the beetles to scale. Additionally, fewer beetles exhibit visible gut distension in July than during other seasons (Griffith and Poulson, 1993). Fresh mass (to 0.1 mg) of individual ova, "whities," and beetles was determined and those samples together with cave cricket carcasses were dried to constant mass at 50-60 C.
Depending on dry mass, individual or pooled samples of cave crickets, cave beetles and cave cricket eggs were weighed to 0.1 mg, digested in 25 or 100 cc volumetric flasks with concentrated [H.sub.2]S[O.sub.4] followed by persulfuric acid, and diluted appropriately. Aliquots were removed, diluted further as needed, and analyzed for nitrogen by Nesslerization (Treybig and Haney, 1983) and for Na and K by flame emission spectrophotometry and for Ca, Mg and total Fe by atomic absorption spectrophotometry with a Varian Spectra AA-20 (Varian Techtron Pty. Ltd., Springvale, Australia). Details of these procedures can be found in Studier and Sevick (1992).
Data were mostly analyzed using SYSTAT (Wilkinson, 1988). For the two sample t-tests that test whether elemental concentrations in eggs differed significantly from predicted mean levels (based on the linear or curvilinear regression relations of nutrient concentrations as a function of dry mass) in newly hatched individuals, variance for predicted means were calculated according to Neter et al. (1985).
RESULTS AND DISCUSSION
Cave crickets of either sex with hind femur lengths [greater than] 19.9 mm are adults (Studier et al., 1986) and are more abundant within populations than any other size class (Studier et al., 1987b). To adjust for multiple comparisons, rejection levels for the null hypotheses tested were reduced from 0.05 to a critical level of 0.01. As shown in previous studies (Studier et al., 1986), adult female cave crickets are heavier than males of similar hind femur length (t = 3.56; P [less than] 0.01; Table 1). While levels of measured minerals did not differ between sexes, N concentrations in males are greater than in females (t = 4.05; P [less than] 0.001). Since surface areas of exoskeletons of male and female cave crickets of the same hind femur length are not different (Studier et al., 1987c), lowered N levels in females strongly imply that the greater, largely internal, mass in females is less N dense than the internal N concentration in carcasses of males.
TABLE 1. - Dry mass (= DM in g) and carcass concentrations of measured elements (mg/g DM) in adult (hind femur lengths [greater than] 19.9 mm) male and female cave crickets, Hadenoecus subterraneus (H. s.). Values shown are mean standard errors of the means. Values in the other Orthoptera column represent arithmetic means for 269 analyzed samples of 300 individuals of 18 different surface orthopteran species (Studier and Sevick, 1992)
Female H. s. Male H. s. Other Orthoptera n 14 15 269
DM 0.1271 0.0073 0.0939 0.0058 0.0994 0.0062 Fe 0.425 0.038 0.327 0.063 0.211 0.023 Mg 1.096 0.051 1.078 0.066 1.340 0.031 K 3.815 0.097 4.105 0.096 12.30 0.18 Ca 3.117 0.400 3.508 0.266 1.876 0.063 Na 1.996 0.133 1.876 0.089 0.659 0.054 N 144.1 1.6 156.6 2.6 163.2 0.2
Gut (crop) contents of cave crickets were removed before carcass composition was determined, whereas gut contents were not removed from other insects. Higher body K and lower body Na levels found in other, epigean orthopterans (t [greater than] 84.3 and t [greater than] 11.7, respectively for both sexes; P [less than] 0.001, in both cases; Table 1) probably reflect levels of those minerals in the plant foods (Weeks, 1978; Dadd, 1985) consumed by such herbivorous insects. The finding that body Mg levels in epigean orthopterans are higher than in cave crickets (t [greater than] 3.59; P [less than] 0.001) is unexpected. In view of the high Mg levels in formations found in caves occupied by Hadenoecus subterraneus in Kentucky and feeding habits that include scavenging, I would expect a greater likelihood of that mineral moving through the food chain in those cave crickets. Higher body Ca levels (t [greater than] 3.06; P [less than] 0.01) found in cave crickets seem to reflect high Ca concentrations in the immediate habitat of cave crickets in Mammoth Cave National Park. A similar explanation applies to cave crickets in which Fe levels are higher than in epigean orthopterans (t = 4.818; P [less than] 0.001). Lower body N levels in cave crickets (t [greater than] 11.87; P [less than] 0.001) are expected. Their more delicate and attenuated exoskeleton would likely contain less protein as well as lower levels of hexosamine polymers, and therefore less N, than more robust, compact surface-dwelling orthopterans.
Since the only difference between genders for any measured element was for N (Table 1), sexes were combined when investigating possible relations of carcass mineral concentrations to body size in cave crickets (Table 2). For each element, 80 samples, some containing several individuals, were analyzed. Hind femur length (HFL) relates very closely to crop empty mass in cave crickets (Studier et al., 1986; Studier and Lavoie, 1996) and either could be used as a size measure. Since regression equations for measured nutrients as functions of crop empty mass do not differ in quality from equations using HFL as the [TABULAR DATA FOR TABLE 2 OMITTED] independent variable and since crickets need not be sacrificed to measure HFL, that measurement is reported as the independent variable for these analyses. Regression equations relating relations of nutrient concentration to dry mass are available upon request from the author.
Carcass Ca concentration is not related to body size in these cave crickets (Table 2). Relationships of carcass Na and K concentrations to body size are marginally significant. Because many regression analyses have been performed, an increased likelihood of type II statistical errors exists and the relationships for Na and K, with their very low coefficients of determination ([r.sup.2]), may be spurious. Body Fe, Mg and N concentrations certainly relate most strongly to size in cave crickets. Total Fe concentration in cave cricket bodies relates curvilinearly to size and increases at HFLs both above and below the calculated (near adult) HFL length of 18.4 mm, where the minimum concentration of Fe (Studier et al., 1975) is 0.296 mg/g dry mass. The relationship for body Mg concentration curves similarly, with minimal concentrations of 0.928 mg/g dry mass in large juvenile cave crickets (HFL = 15.7 mm). Body N concentrations [ILLUSTRATION FOR FIGURE 1 OMITTED] decrease linearly with size in males but decrease curvilinearly in females so that differences between sexes appear in adult crickets. This observation supports the previous speculation that lower body N levels in females relate to lower N levels in reproductive tract biomass.
Linear relationships between measured elements and body size in cave crickets can be compared to five other species of orthopterans (Studier and Sevick, 1992). In view of low coefficients of determination and tenuous relationships for Na and K to size in cave crickets (Table 2), no strong relationships typically exist between body mineral concentrations and body size in cave crickets or other orthopterans. In those rare instances where mineral concentrations do relate to body size, the variables typically are inversely related. Of all measured elements, the inverse relationship is strongest for body N levels and probably reflects decreasing surface area to body mass ratios that routinely accompany increasing size.
Levels of N in eggs (Table 3) are significantly lower (t = 18.85; P [less than] 0.01) than N levels in hatchlings of similar dry mass (standard errors for egg compositions are given in Table 4). Since some adult female cave crickets are gravid in nearly all seasons and since the reproductive tract biomass of females is much greater than in males (Studier et al., 1986), presence of ova in the bodies of adult females lowers their average N concentration and explains the lower N level found in adult female cave crickets, compared to adult males. No differences are seen in K, Fe and Mg levels between cricket eggs and hatchlings; however, concentrations of Ca in hatchlings are significantly lower than for eggs (t = 7.16; P [less than] 0.01), whereas Na levels in hatchlings significantly exceed egg Na concentrations (t = 6.95; P [less than] 0.01). Although no data comparing N or mineral composition differences of eggs vs. hatchlings in other insects have been located, such differences in composition of biomass are not uncommon when comparing other stages in the life history of insects (Slansky and Scriber, 1985; Studier et al., 1991). My data for cave crickets indicate that the shell and other extraembryonic biomass contain significantly more Ca and significantly less N and Na than bodies of hatchlings. A similar marked reduction in Ca and increase in N level accompanies metamorphosis in tent moths (Studier et al., 1991).
TABLE 3. - Average concentrations (mg/g dry mass) of nitrogen and selected minerals in cave cricket eggs (= Eggs, average from 12 pooled samples) and hatchlings (= Hatch, average from five pooled samples) and in bodies of the cave beetle, Neaphaenops tellkampfi (= Cave, 18 samples) and other, noncavernicolous beetles (= Others, 43 species, 194 samples)
Element Eggs Hatch Cave Others
Iron 1.027 2.104 0.933 0.188 Magnesium 1.155 1.822 0.739 1.523 Potassium 3.56 3.55 2.87 9.01 Calcium 4.839 4.602 5.133 1.050 Sodium 1.104 0.863 1.633 1.660 Nitrogen 108.8 166.3 119.4 163.2
[TABULAR DATA FOR TABLE 4 OMITTED]
The second primary component of this study compares N and mineral composition of carcasses of the troglobitic cave beetle, Neaphaenops tellkampfi, a specialist on eggs of cave crickets, to other beetles and to cave cricket eggs. Using data found in Studier and Sevick (1992) for comparison, we found that levels of Ca and Fe in Neaphaenops are significantly higher than in other epigean beetles (t = 32.3 and 8.53, respectively, P [less than] 0.001 in each case) and other carabids (t = 17.3 and 5.75, respectively, P [less than] 0.001 in each case), are more similar to levels of these elements found in cave cricket eggs and may also relate to abundance of those minerals in the cave habitat (Table 3). Lower carcass K levels (t = 27.8 and 9.87; P [less than] 0.001 in both cases for other epigean beetles and other carabids, respectively) in Neaphaenops would be due to greater direct or indirect (by eating herbivorous prey) ingestion of plant foods by epigean beetles. In view of the abundance of Mg in the cave environment of Neaphaenops, lower concentrations of Mg in cave beetle carcasses compared to epigean beetles (t = 16.4; P [less than] 0.001), however, is unexpected; however, body Mg concentrations in Neaphaenops do not differ from other carabids (t = 2.00, P [greater than] 0.05). Concentrations of N in Neaphaenops carcasses, which are very much lower (t = 16.9 and 7.32, P [less than] 0.001 in both cases) than in other epigean beetles or other carabids, correspond to the low N content in cave cricket eggs and also reflect the general adaptation of this beetle to a troglobitic existence.
Dry mass values show that, while Neaphaenops is larger than a cave cricket egg, cave cricket eggs, at about 75% of the beetle's mass, represent a huge meal (Table 4). Such exceptionally large (1.7% of the adult mass of a cave cricket) eggs are often seen in cave-adapted insects. Although N levels in the body of Neaphaenops are significantly higher than in cave cricket eggs (Table 4), carcass N level in this beetle is much more similar to cave cricket eggs than to epigean beetles (Table 3). While no differences are seen in Fe and Ca levels of Neaphaenops bodies and cave cricket eggs (Table 4), lower K and higher Na levels in Neaphaenops carcasses may simply be because these insects are one step further removed in any food chain from herbivores and their high K, low Na diets. Cave crickets generally forage outside the cave, consuming fungi and scavenging other available items as well as ingesting fresh and preprocessed (as livestock dung) plant material. Concentrations of elements measured in carcasses of Neaphaenops differ considerably from surface-dwelling beetles (including carabids) and are more similar in composition to the cave cricket eggs upon which they feed. In regard then to the concept of "you are what you eat," the carcass composition of Neaphaenops is certainly affected by the composition of what they eat and is more similar to cave cricket eggs than to the bodies of other beetles.
Using previously established rates of egg laying of 0.25 to 1.0/day (Cyr et al., 1991), egg dry mass average (Table 4), egg caloric density of 5.59 cal/mg dry mass and energy assimilated by adult female Hadenoecus subterraneus of 1.06 cal/h (both from Studier et al., 1986), the fraction of the daily energy budget devoted, by adult female cave crickets, to egg growth ranged from 12.4 to 49.6% of daily assimilated energy. That highly variable estimate compares favorably to the wide comparable range (reviewed by Slansky and Scriber, 1985) of 0% in some lepidopterans that don't eat as adults to 68.3% in one hemipteran. Values reported by those authors are 36.2% for a single (epigean) orthopteran species and 4.7, 39.1 and 39.3% in three curculionid coleopteran species. In view of those limited and highly variable data, speculations about the ecological or physiological significance in comparing epigean with cave-adapted insects are certainly premature.
While very few comparable data are available, tentative growth rates of cave crickets can be estimated. Dry masses of eggs and adult cave crickets have been determined (Tables 1 and 4). Previous data collected at study sites in Mammoth Cave National Park by T. Poulson (pers. comm.) suggest that 2 yr are likely needed for hatchlings to grow to adult size. Using that estimate of time span needed for growth, estimates of dry mass growth rates can be made. Since adult male cave crickets are smaller than adult females, dry mass accretion rates are less in males than in females. Absolute growth rates for males and females average 0.13 and 0.17 mg dry mass/day, respectively. Solving the individual growth rate equation for poikilotherms attributed to Farlow by Peters (1983) and using caloric densities we reported for Hadenoecus subterraneus (Studier et al., 1986), calculated absolute growth rates for these cave crickets are 1.1 and 1.3 mg/day for males and females, respectively. Relative growth rates (mg dry mass/day [mg.sup.-1] dry body mass) reviewed for many epigean insects by Slansky and Scriber (1985) range from 0.03 to 0.50. Similar (minima and maxima) calculations for cave crickets range from 0.0013 to 0.055 and 0.0014 to 0.076, for males and females, respectively. Growth rates for dry mass in cave crickets are, therefore, slower by approximately one order of magnitude than would be expected in other insects. Such slow growth rates are generally characteristic of cave-adapted organisms (Poulson and White, 1969; Culver, 1982).
In addition to growth rates of dry mass, rates of accretion for other measured nutrients have also been estimated (Table 5). Since measured nutrients are expressed as functions of dry body mass (Table 2), accretions for each nutrient are direct functions of growth rates of dry body mass. Inadequate data on nutrient accretions in insects are available for comparison. Since growth rates of dry body mass in cave crickets are roughly 0.1 the rates in other insects, N and mineral accretion rates (Table 5) are similarly expected to be much slower than in epigean insects.
Estimates of nutrient mass needed for egg production in cave crickets (Table 5) are based on a minimum to maximum estimate of production of 1 egg/4 days to 1 egg/day (Cyr et al., 1991). As is true for measured nutrients in carcasses, no data on egg mineral levels are available for comparison. With the possible exception of Na, daily requirements for egg growth greatly exceed maximal nutrient requirements for body growth. For daily growth of both body and eggs, N requirements exceed mineral requirements by at least one order of magnitude.
TABLE 5. - Estimated maximal rate of daily accretion (micrograms/ day) of measured elements (= Element) starting from newly hatched cave crickets growing to adult size in 1 yr for male (= Male) and female (= Female) cave crickets. Since cave crickets may require 2 or more yr to reach adult size, values shown may be too high by a factor of 2 or more. Estimated daily requirement (micrograms/day) for rates of maximal (Max) and minimal (Min) egg production in adult female cave crickets
Cave crickets Required for eggs
Element Male Female Max Min
Iron 0.0777 0.142 2.3 20.58 Magnesium 0.272 0.313 2.61 0.65 Potassium 1.04 1.31 8.03 2.01 Calcium 0.871 1.06 10.9 2.73 Sodium 0.476 0.688 2.49 0.62 Nitrogen 39.6 49.5 245. 61.2
Acknowledgments. - I thank Dr. K. Lavoie and J. Dakki for collecting the N. tellkampfi and Mark Deevey and Leonard Nowak who aided in some respects of field and laboratory work. Dr. R. Podolsky aided in data analyses. Drs. K. Lavoie and T. Poulson and D. Viele provided many useful comments on this manuscript. I thank the National Park Service personnel and the Cave Research Foundation for use of facilities at Mammoth Cave National Park.
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|Author:||Studier, Eugene H.|
|Publication:||The American Midland Naturalist|
|Date:||Jul 1, 1996|
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