Features Relevant to Invertebrate Sentience, Part 2

Ex­ec­u­tive Summary

In this, the sec­ond of three posts on fea­tures po­ten­tially rele­vant to in­ver­te­brate sen­tience, we as­sess 5 drug re­sponses, 5 mo­ti­va­tional trade­offs, and 5 feats of cog­ni­tive so­phis­ti­ca­tion. Here are some high-level take­aways:

  1. Re­search that an­a­lyzes the effects of anal­gesics, an­tide­pres­sants, and anx­iolyt­ics on in­ver­te­brates—es­pe­cially self-ad­minis­tra­tion stud­ies—has the po­ten­tial to re­veal im­por­tant ev­i­dence about var­i­ous in­ver­te­brates’ ca­pac­ity for valenced ex­pe­rience.

  2. Study­ing mo­ti­va­tional trade­offs can help us dis­t­in­guish re­flex­ive, pre-pro­grammed be­hav­iors from more plas­tic re­sponses.

  3. Com­par­ing cog­ni­tive so­phis­ti­ca­tion across dis­similar taxa is ex­traor­di­nar­ily difficult.

  4. Notwith­stand­ing (3), many in­ver­te­brates, es­pe­cially arthro­pods and cephalopods, ap­pear sur­pris­ingly in­tel­li­gent.

  5. The re­la­tion­ship be­tween cog­ni­tive so­phis­ti­ca­tion and the ca­pac­ity for valenced ex­pe­rience is un­clear.

In­tro­duc­tion and Pro­ject Overview

This post is the fourth in Re­think Pri­ori­ties’ se­ries on in­ver­te­brate[1] welfare. In the first post we ex­am­ine some philo­soph­i­cal difficul­ties in­her­ent in the de­tec­tion of morally sig­nifi­cant pain and plea­sure in non­hu­mans. In the sec­ond post we dis­cuss our sur­vey and com­pila­tion of the ex­tant sci­en­tific liter­a­ture rele­vant to in­ver­te­brate sen­tience,[2] as well as the strengths and weak­nesses of our ap­proach to the sub­ject. In the third post we ex­plain some anatom­i­cal, evolu­tion­ary, and be­hav­ioral fea­tures po­ten­tially in­dica­tive of the ca­pac­ity for con­scious ex­pe­rience in in­ver­te­brates. In this post we ex­plain some drug re­sponses, mo­ti­va­tional trade­offs, and feats of cog­ni­tive so­phis­ti­ca­tion po­ten­tially in­dica­tive of the ca­pac­ity for con­scious ex­pe­rience in in­ver­te­brates. In the fifth post we ex­plain some learn­ing in­di­ca­tors, nav­i­ga­tional skills, and mood state be­hav­iors po­ten­tially in­dica­tive of the ca­pac­ity for con­scious ex­pe­rience in in­ver­te­brates. In the sixth, sev­enth, and eighth posts, we pre­sent our sum­mary of find­ings, both in nar­ra­tive form and as an in­ter­ac­tive database. In forth­com­ing work, to be pub­lished in late July, we an­a­lyze the ex­tent to which in­ver­te­brate welfare is a promis­ing cause area.

Drug Responses

Affected by anal­gesics in a man­ner similar to humans

An anes­thetic is a sub­stance which in­duces a gen­eral lack of feel­ing in the tar­get area. In con­trast, an anal­gesic speci­fi­cally re­duces the sen­sa­tion of pain with­out elimi­nat­ing other feel­ings. In hu­mans var­i­ous types of anal­gesics are used as painkil­lers. Study­ing the effects of anal­gesics on in­ver­te­brates may help us bet­ter un­der­stand if they pos­sess the ca­pac­ity for valenced ex­pe­rience. Of course, there’s no way to di­rectly mea­sure if an anal­gesic re­duces pain sen­sa­tion in a non­hu­man an­i­mal, so we have to look for prox­ies. One such proxy is a re­duc­tion in no­ci­cep­tive re­flexes and avoidant be­hav­ior. If non­hu­man an­i­mals re­act to anal­gesics with diminished no­ci­cep­tive re­flexes and avoidant be­hav­ior, then, in the ab­sence of defeaters, that is ev­i­dence that the anal­gesics are act­ing to re­duce pain in the an­i­mals.

One must be care­ful to dis­t­in­guish be­tween cases in which no­ci­cep­tive re­flexes and avoidant be­hav­ior are re­duced from cases in which ac­tivity over­all is re­duced. There is a huge va­ri­ety of anal­gesics and their effects on phy­lo­ge­net­i­cally dis­tant an­i­mals is largely un­known. If a par­tic­u­lar anal­gesic func­tions more like an anes­thetic, re­duc­ing over­all sen­sa­tion, no­ci­cep­tive re­flexes and avoidant be­hav­ior may be diminished—but for the wrong rea­sons. Similarly, an anal­gesic might merely dam­age an an­i­mal, lead­ing to re­duced ac­tivity with­out any sup­pres­sion of pain.[3] One pos­si­ble way to cir­cum­vent these wor­ries is to test cases in which, if the anal­gesic did provide pain re­lief, the an­i­mal would in­crease rather than de­crease ac­tivity, for ex­am­ple when the sen­sa­tion of pain might cau­tion an an­i­mal against tak­ing a par­tic­u­lar ac­tion.

Self-ad­ministers analgesics

Self-ad­minis­tra­tion stud­ies may help us bet­ter un­der­stand whether an anal­gesic re­duces pain sen­sa­tion or merely diminishes re­sponse to stim­uli in gen­eral. In (the rele­vant sub­set of) self-ad­minis­tra­tion stud­ies, in­jured an­i­mals are given the op­por­tu­nity to feed or drink from a source laced with an anal­gesic or a con­trol source with no added drugs. Self-ad­minis­tra­tion stud­ies have been performed on a va­ri­ety of an­i­mals from rats[4] to chick­ens[5] to hon­ey­bees.[6] When the an­i­mals in these stud­ies fa­vor the anal­gesic source, that is mild ev­i­dence that their in­juries cause them pain for which they seek re­lief. When the an­i­mals show no prefer­ence for the anal­gesic source, that is mild ev­i­dence that ei­ther the in­jured an­i­mals are not in pain or that the anal­gesic does not re­duce their pain. Of course, con­found­ing fac­tors must be con­sid­ered. Per­haps the anal­gesic al­ters the taste of the food/​wa­ter so much that it makes the food/​wa­ter un­palat­able de­spite its pain-re­liev­ing prop­er­ties. And as noted above, there is an as­tound­ing ar­ray of available anal­gesics. The fact that one type of anal­gesic does not re­duce the pain as­so­ci­ated with one type of in­jury does not prove that anal­gesics in gen­eral don’t re­lieve pain or that the an­i­mals in the study are in­ca­pable of valenced ex­pe­rience.

Affected by recre­ational drugs in a man­ner similar to humans

A wide va­ri­ety of recre­ational drugs have been tested on in­ver­te­brates, in­clud­ing am­phetamine in crayfish,[7] co­caine in honey bees,[8] mar­ijuana and caf­feine in spi­ders,[9] and MDMA in oc­to­puses.[10] In hu­mans, recre­ational drugs of­ten al­ter the valence of ex­pe­rience. If when ex­posed to these drugs non­hu­man an­i­mals ex­hibit be­hav­ior rele­vantly similar to the be­hav­ior of hu­mans ex­posed to the same drugs, then, in the ab­sence of defeaters, we have some ev­i­dence that those non­hu­man an­i­mals un­dergo similarly valenced ex­pe­riences. Of course, not all changes in be­hav­ior are the re­sult of changes in valenced ex­pe­rience. Re­cre­ational drugs are of­ten toxic, and some changes in be­hav­ior, both in hu­mans and non­hu­mans, are the re­sult of the body re­act­ing to a poi­son. It’s pos­si­ble that neu­ro­chem­i­cal mark­ers can help us dis­t­in­guish be­hav­ioral changes caused by changes in valenced ex­pe­rience from be­hav­ioral changes caused by changes in phys­iol­ogy.[11]

Like many other fea­tures we in­ves­ti­gated, this fea­ture comes in de­grees, in this case along at least two di­men­sions. The first and most ob­vi­ous di­men­sion is similar­ity to hu­man be­hav­ior. Similar­ity is not bi­nary. Some re­ac­tions to recre­ational drugs will be more similar to hu­man re­ac­tions than oth­ers. Even set­ting aside the prob­lem of mea­sur­ing similar­ity, it’s difficult to know what de­gree of similar­ity should be suffi­cient for a crea­ture to be said to pos­sess this fea­ture.

The other di­men­sion con­cerns the num­ber of drugs that af­fect a crea­ture in a man­ner similar to hu­mans. A crea­ture may re­act to some recre­ational drugs in a man­ner similar to hu­mans and re­act to other recre­ational drugs in a to­tally non-hu­man man­ner. Crea­tures that re­act to more recre­ational drugs in a man­ner similar to hu­mans might be said to bet­ter satisfy this fea­ture than crea­tures that re­act to fewer recre­ational drugs in a man­ner similar to hu­mans. How­ever, for pur­poses of this pro­ject, we counted a crea­ture as pos­sess­ing this fea­ture so long as it re­acts to at least one recre­ational drug in a man­ner similar to hu­mans.

This fea­ture is con­sid­er­ably more am­bigu­ous than many of the other fea­tures we in­ves­ti­gated. We have not at­tempted to define “recre­ational drug” with much pre­ci­sion, and hence there will in­evitably be edge cases that are difficult to clas­sify. (For in­stance, should we in­clude codeine and other medicines that are abused recre­ation­ally? We’re not sure.) More wor­ry­ingly, we have not delineated in ad­vance which be­hav­ioral and phys­iolog­i­cal changes would qual­ify as a re­ac­tion rele­vantly similar to a hu­man re­ac­tion. Given the huge num­ber of recre­ational drugs and their in­cred­ible ar­ray of po­ten­tial effects, it would be difficult for us to spec­ify ex­actly what re­ac­tions to look for. In­stead, we’ve had to rely on at­tri­bu­tions of similar­ity in the liter­a­ture. So, for ex­am­ple, in a re­cent study on the effects of al­co­hol on the ne­ma­tode C. el­e­gans, the au­thors re­port that the round­worm dis­plays dis­in­hibited lo­co­mo­tion and feed­ing be­hav­iors af­ter be­ing ex­posed to ethanol. They write, “Similar be­hav­ioral dis­in­hi­bi­tion is also seen in many an­i­mal mod­els of ethanol re­sponse, from in­ver­te­brates to mam­mals and pri­mates.”[12] Thus, we con­cluded that C. el­e­gans is af­fected by (at least one) recre­ational drug in a man­ner similar to hu­mans.

Self-ad­ministers recre­ational drugs

Self-ad­minis­tra­tion stud­ies may help us bet­ter un­der­stand whether recre­ational drugs al­ter be­hav­ior due to changes in valenced ex­pe­rience or merely due to changes in phys­iol­ogy. In (the rele­vant sub­set of) self-ad­minis­tra­tion stud­ies, an­i­mals are given the op­por­tu­nity to feed or drink ei­ther from sources laced with recre­ational drugs or un­altered con­trol sources.[13] If the an­i­mals con­sis­tently pre­fer the source laced with recre­ational drugs, that is some ev­i­dence that they find the effects of the drug plea­surable, and hence have a ca­pac­ity for valenced ex­pe­rience.

Of course, there are a num­ber of com­pli­ca­tions which must be ac­counted for when eval­u­at­ing the im­por­tance of this fea­ture. First, the recre­ational drug may al­ter the taste of the food/​wa­ter so much that it makes the food/​wa­ter un­palat­able de­spite its plea­sure-in­duc­ing prop­er­ties. Thus, a crea­ture’s failure to self-ad­minister a recre­ational drug does not pre­clude the pos­si­bil­ity that the crea­ture finds the drug plea­surable. Se­cond, some recre­ational drugs are highly ad­dic­tive. If an or­ganism be­gins a self-ad­minis­tra­tion study con­sum­ing equal quan­tities of the ex­per­i­men­tal and con­trol source, it may quickly be­come ad­dicted to the ex­per­i­men­tal source and al­ter its be­hav­ior ac­cord­ingly. Im­por­tantly, the pro­cess of al­ter­ing one’s be­hav­ior in re­sponse to an ad­dic­tive sub­stance need not in­volve any con­scious ex­pe­rience—even in hu­mans. In lab­o­ra­tory set­tings hu­man ad­dicts will dis­play a sub­con­scious prefer­ence for in­tra­venous doses of co­caine too small to pro­duce con­scious effects. The ad­dicts do not re­port any differ­ences in sub­jec­tive feel­ing and deny that they are ex­press­ing a prefer­ence at all.[14] Hence, self-ad­minis­tra­tion be­hav­ior need not be driven by the ca­pac­ity for valenced ex­pe­rience.

Affected by an­tide­pres­sants or anx­iolyt­ics in a man­ner similar to humans

The effects of an­tide­pres­sant and anx­iolytic[15] drugs have been ex­plored in a num­ber of in­ver­te­brate species, in­clud­ing fruit flies,[16] ne­ma­todes,[17] and crabs.[18] In hu­mans, an­tide­pres­sant and anx­iolytic drugs al­ter the valence of ex­pe­rience. If when ex­posed to these drugs non­hu­man an­i­mals ex­hibit be­hav­ior rele­vantly similar to the be­hav­ior of hu­mans ex­posed to the same drugs, then, in the ab­sence of defeaters, we have some ev­i­dence that those non­hu­man an­i­mals un­dergo similarly valenced ex­pe­riences. Of course, not all changes in be­hav­ior are the re­sult of changes in valenced ex­pe­rience. An­tide­pres­sant and anx­iolytic drugs may be toxic to some an­i­mals, and thus some be­hav­ioral changes in non­hu­mans may be me­di­ated solely by phys­iolog­i­cal changes.[19] Hope­fully, neu­ro­chem­i­cal anal­y­sis can help us dis­t­in­guish be­hav­ioral changes caused by changes in valenced ex­pe­rience from be­hav­ioral changes caused by changes in phys­iol­ogy.

An ex­am­ple will help illus­trate this fea­ture. Ac­cord­ing to a 2014 study, stress-in­duced avoidance be­hav­ior in crayfish bears a strik­ing re­sem­blance to mam­malian anx­iety.[20] The au­thors demon­strate that shocked crayfish de­velop an ex­tended, con­text-in­de­pen­dent aver­sion to light. (The shocks were not as­so­ci­ated with lev­els of illu­mi­na­tion.) In con­trast, un­shocked crayfish, though prefer­ring the dark, were happy to ex­plore both illu­mi­nated and unillu­mi­nated ar­eas of their en­vi­ron­ment. Most im­por­tantly, in­ject­ing the crayfish with the anx­iolytic drug chlor­diazepox­ide (used to treat anx­iety in hu­mans) elimi­nated the aver­sion to light.[21] In hu­mans, anx­iety is of­ten as­so­ci­ated with dan­ger that is per­ceived to be un­avoid­able or situ­a­tions in which the threat is am­bigu­ous or un­known. The elec­tric shocks ap­plied to the crayfish fit this de­scrip­tion. In hu­mans, anx­iety is as­so­ci­ated with gen­er­al­ized fear, that is, in­creased fear of un­re­lated stim­uli. The shocked crayfish ap­peared to ex­hibit in­creased fear of light that is un­re­lated to the source of stress. In hu­mans, anx­iety is re­duced by anx­iolytic drugs. In crayfish, anx­iety-like be­hav­ior is re­duced by anx­iolytic drugs. One ex­pla­na­tion of this phe­nomenon is that crayfish, like hu­mans, are ca­pa­ble of ex­pe­rienc­ing nega­tively valenced emo­tional states.

Like many other fea­tures we in­ves­ti­gated, this fea­ture comes in de­grees, in this case along at least two di­men­sions. The first and most ob­vi­ous di­men­sion is similar­ity to hu­man be­hav­ior. Similar­ity is not bi­nary. Some re­ac­tions to an­tide­pres­sant and anx­iolytic drugs will be more similar to hu­man re­ac­tions than oth­ers. Even set­ting aside the prob­lem of mea­sur­ing similar­ity, it’s difficult to know what de­gree of similar­ity should be suffi­cient for a crea­ture to be said to pos­sess this fea­ture.

The other di­men­sion con­cerns the num­ber of drugs that af­fect a crea­ture in a man­ner similar to hu­mans. A crea­ture may re­act to some an­tide­pres­sant and anx­iolytic drugs in a man­ner similar to hu­mans and re­act to other an­tide­pres­sant and anx­iolytic drugs in a to­tally non-hu­man man­ner. Crea­tures that re­act to more an­tide­pres­sant and anx­iolytic drugs in a man­ner similar to hu­mans might be said to bet­ter satisfy this fea­ture than crea­tures that re­act to fewer an­tide­pres­sant and anx­iolytic drugs in a man­ner similar to hu­mans. How­ever, for pur­poses of this pro­ject, we counted a crea­ture as pos­sess­ing this fea­ture so long as it re­acts to at least one an­tide­pres­sant and anx­iolytic drug in a man­ner similar to hu­mans.

Fi­nally, it should be noted that we were not able to find enough stud­ies to in­clude the fea­ture self-ad­ministers an­tide­pres­sant or anx­iolytic drugs on the table.

Mo­ti­va­tional Tradeoffs

Pay­ing a cost to re­ceive a reward

An an­i­mal pos­sesses this fea­ture if it can and will sac­ri­fice some­thing of im­me­di­ate value in or­der to earn a pos­i­tive stim­u­lus.[22] Many an­i­mals, in­clud­ing at least one species of in­ver­te­brate, are will­ing to pay a cost to re­ceive a re­ward. For ex­am­ple, fruit flies will en­dure elec­tric shock in or­der to at­tain the cue as­so­ci­ated with ethanol, in­di­cat­ing that they are pre­pared to tol­er­ate pun­ish­ment to ob­tain the drug.[23] This be­hav­ior sug­gests fruit flies are ca­pa­ble of weigh­ing com­pet­ing in­ter­ests. In gen­eral, mo­ti­va­tional trade­off be­hav­ior is ev­i­dence that the an­i­mal in ques­tion pos­sesses some kind of unified util­ity func­tion in which benefits and risks of differ­ent types are pro­cessed and eval­u­ated. This type of in­te­gra­tion may be ev­i­dence for the ca­pac­ity for valenced ex­pe­rience.

Of course, some trade­off be­hav­ior is sure to be purely re­flex­ive, in­stinc­tual, or oth­er­wise pre-pro­grammed. The con­text in which an an­i­mal dis­plays this trait is im­por­tant for de­ter­min­ing the im­por­tance of the fea­ture.[24] Trade­off be­hav­ior that oc­curs in novel situ­a­tions demon­strates the plas­tic­ity that one would ex­pect of a crea­ture with the ca­pac­ity for valenced ex­pe­rience. Trade­off be­hav­ior that oc­curs in re­sponse to situ­a­tions re­peat­edly en­coun­tered in the wild does not re­quire the same level of plas­tic­ity and hence may not re­quire the ca­pac­ity for valenced ex­pe­rience.

Pay­ing a cost to avoid a nox­ious stimulus

An an­i­mal pos­sesses this fea­ture if it can and will sac­ri­fice some­thing of im­me­di­ate value to pre­vent or halt a nox­ious event. Many an­i­mals, in­clud­ing in­ver­te­brates, are will­ing to pay a cost to avoid a nox­ious stim­u­lus. For in­stance, shore crabs gen­er­ally avoid well-lit ar­eas, prefer­ring to hide in dark en­vi­ron­ments such as those found un­der rocks. Given the choice be­tween two cham­bers in a lab­o­ra­tory set­ting, one brightly lit and the other dark, the crabs will uni­ver­sally choose the dark cham­ber. How­ever, if the dark cham­ber is rigged to de­liver a mild shock, the crabs will be­gin to opt for the nor­mally avoided well-lit cham­ber. The crabs do so in in­creas­ing num­bers (and in­creas­ingly quickly) as the num­ber of tri­als in­creases.[25] A com­pel­ling ex­pla­na­tion of this be­hav­ior is that the crabs feel pain, then learn to avoid the pain by choos­ing the op­po­site, oth­er­wise un­de­sir­able cham­ber.

Of course, some trade­off be­hav­ior is sure to be purely re­flex­ive, in­stinc­tual, or oth­er­wise pre-pro­grammed. The con­text in which an an­i­mal dis­plays this trait is im­por­tant for de­ter­min­ing the im­por­tance of the fea­ture. Trade­off be­hav­ior that oc­curs in novel situ­a­tions demon­strates the plas­tic­ity that one would ex­pect of a crea­ture with the ca­pac­ity for valenced ex­pe­rience. Trade­off be­hav­ior that oc­curs in re­sponse to situ­a­tions re­peat­edly en­coun­tered in the wild does not re­quire the same level of plas­tic­ity and hence may not re­quire the ca­pac­ity for valenced ex­pe­rience.

Self-control

For our pur­poses, self-con­trol is the abil­ity to con­sis­tently choose a large de­layed re­ward over a small im­me­di­ate re­ward. Self-con­trol re­quires some form of pro­cess­ing in which differ­ent needs and de­sires are weighed against each other.[26] Self-con­trol prob­a­bly can­not be ex­er­cised re­flex­ively. Thus, self-con­trol is ev­i­dence of be­hav­ioral plas­tic­ity, which is it­self mod­est ev­i­dence for the ca­pac­ity for valenced ex­pe­rience.

Self-con­trol has been stud­ied ex­ten­sively in ver­te­brates, in­clud­ing hu­mans.[27] Pi­geons and rats con­sis­tently demon­strate a prefer­ence for im­me­di­ate small re­wards over large de­layed re­wards. This im­pul­sive­ness may have an evolu­tion­ary ex­pla­na­tion. In en­vi­ron­ments where an­i­mals face un­cer­tain fu­tures, opt­ing for a more cer­tain small re­ward may be more benefi­cial than wait­ing for a larger re­ward which may not come. Self-con­trol has only re­cently been stud­ied in in­ver­te­brates. Eu­so­cial in­sects, such as bees and ants, would ap­pear to benefit from self-con­trol. Be­cause work­ers are in­fer­tile, prop­a­gat­ing work­ers’ genes re­quires the long-term sur­vival of the hive or colony. Ini­tial in­di­ca­tions sug­gest that honey bees choose large de­layed re­wards over small im­me­di­ate re­wards at much greater rates than rats and pi­geons.[28]

Preda­tor avoidance tradeoffs

To stay al­ive, an­i­mals must avoid preda­tors. To stay al­ive, an­i­mals must eat and drink. Some­times, the need to avoid preda­tors con­flicts with the need to eat and drink. In these cases, the an­i­mal must weigh com­pet­ing de­mands and come to a de­ci­sion. Such preda­tor avoidance trade­offs have been widely stud­ied, in­clud­ing in in­ver­te­brates. Earth­worms will feed in high-light con­di­tions (ex­pos­ing them both to vi­sual preda­tors and the threat of dessi­ca­tion) when they are starved and half-starved but not when they are fully nour­ished.[29] Over­head shad­ows (in­di­cat­ing a po­ten­tial preda­tor) cause fully nour­ished fruit flies to dis­perse, but starved fruit flies re­main feed­ing.[30] In a lab­o­ra­tory set­ting, her­mit crabs will aban­don their shells if they are sub­jected to a mild shock. How­ever, the crabs are sig­nifi­cantly less likely to aban­don their shells af­ter shock if the odor of a preda­tor is pre­sent.[31]

Like other mo­ti­va­tional trade­offs, some preda­tor avoidance trade­off be­hav­ior is likely to be re­flex­ive and hard­wired. Nearly all an­i­mals, even very sim­ple crea­tures, must bal­ance the risk of star­va­tion and the risk of pre­da­tion. Take no risks when near­ing star­va­tion and the an­i­mal will starve to death. Take too many risks when already nour­ished and an an­i­mal may die with­out re­duc­ing risk from star­va­tion. Thus, it could be ar­gued, hav­ing some varied re­sponse in these sce­nar­ios would be ex­pected given evolu­tion­ary se­lec­tion pres­sures re­gard­less of the pres­ence or ab­sence of men­tal states of any kind.[32]

Some con­texts, how­ever, can provide ev­i­dence for the ca­pac­ity for valenced ex­pe­rience. When con­sid­er­ing shocked her­mit crabs leav­ing their shells, it is tempt­ing to con­clude that the be­hav­ior is purely re­flex­ive. How­ever, the fact that the crabs re­main in their shells when the odor of a preda­tor is pre­sent sug­gests that the be­hav­ior is not re­flex­ive. A nat­u­ral ex­pla­na­tion is that the crabs weigh the pain of the shock against the fear of a preda­tor. In the ab­sence of defeaters, it may be more par­si­mo­nious to pre­fer this ex­pla­na­tion to al­ter­na­tive ex­pla­na­tions.

Selec­tive at­ten­tion to nox­ious stim­uli over other con­cur­rent events

The de­gree to which a nox­ious event com­mands the at­ten­tion of an an­i­mal can po­ten­tially tell us some­thing about whether that event is ex­pe­rienced as painful or not. In hu­mans the con­scious sen­sa­tion of pain is dis­tract­ing.[33] Mild pain can be an an­noy­ance, and in­tense pain can be so over­whelming that it effec­tively in­ca­pac­i­tates the sufferer. If a non­hu­man an­i­mal de­votes more at­ten­tion to a nox­ious event than other po­ten­tial ob­jects of at­ten­tion, es­pe­cially if do­ing so re­duces rather than in­creases an an­i­mal’s fit­ness, that is ev­i­dence that the nox­ious event is ex­pe­rienced as painful. In con­trast, if an an­i­mal com­pletely ig­nores a nox­ious event, that is ev­i­dence that the nox­ious event is not ex­pe­rienced as painful. For ex­am­ple, male man­tids will con­tinue to mate even as they are de­voured by their part­ners.[34] This be­hav­ior has a clear evolu­tion­ary ex­pla­na­tion. Only by mat­ing suc­cess­fully can the male man­tid’s genes prop­a­gate. Nonethe­less, it is hard to imag­ine any mam­malian male con­tin­u­ing to mate while it is be­ing eaten al­ive; the pain would be too dis­tract­ing. Hence, it seems the male man­tid doesn’t ex­pe­rience the pro­cess of be­ing eaten al­ive as painful.[35] Per­haps it doesn’t ex­pe­rience any­thing as painful.

Cog­ni­tive Sophistication

Uncer­tainty monitoring

An an­i­mal en­gages in un­cer­tainty mon­i­tor­ing when it is aware, in a rough and min­i­mally func­tional sense, of its cre­dence in a par­tic­u­lar propo­si­tion. Hu­mans en­gage in un­cer­tainty mon­i­tor­ing with rel­a­tive ease. Asked to name both the 22nd pres­i­dent of the United States and the 1st pres­i­dent of the United States, most hu­mans have lit­tle prob­lem iden­ti­fy­ing which an­swer they are more con­fi­dent in. Even three-year-old chil­dren are ca­pa­ble of un­cer­tainty mon­i­tor­ing.[36]

For most of the 20th cen­tury, it was thought that un­cer­tainty mon­i­tor­ing was a skill unique to hu­mans. In the mid-1990s, re­searchers be­gan ap­ply­ing the so-called “un­cer­tain re­sponse” paradigm to non­hu­man an­i­mals. In an un­cer­tain re­sponse paradigm, an­i­mals are trained to as­so­ci­ate a cor­rect an­swer to some ques­tion with a re­ward and an in­cor­rect an­swer with a pun­ish­ment. A third an­swer choice is then in­tro­duced: un­cer­tain. If an an­i­mal re­sponds with the un­cer­tain an­swer, it re­ceives nei­ther pun­ish­ment nor re­ward. When pre­sented with a se­ries of in­creas­ingly difficult ques­tions, an­i­mals ca­pa­ble of un­cer­tainty mon­i­tor­ing will se­lect the un­cer­tain re­sponse where ap­pro­pri­ate, thereby im­prov­ing their over­all re­ward-to-pun­ish­ment ra­tio. Us­ing this paradigm, un­cer­tainty mon­i­tor­ing has been con­clu­sively demon­strated in both dolphins and rhe­sus mon­keys.[37]

Re­cently, un­cer­tainty mon­i­tor­ing has been stud­ied in eu­so­cial in­sects. Us­ing the paradigm out­lined above, one study tasked honey bees with dis­crim­i­nat­ing be­tween two stim­uli. A cor­rect an­swer earned a re­ward (su­crose) and an in­cor­rect an­swer earned a pun­ish­ment (qui­nine). When given the choice to opt out, honey bees were found to opt out more of­ten when the trial was difficult (when the honey bee was pro­por­tionately more likely to re­ceive a pun­ish­ment than a re­ward). The honey bees on av­er­age im­proved their suc­cess-to-failure ra­tio when given the op­tion to opt out of tri­als.[38]

Another study found that ants up­reg­u­late pheromone trail de­po­si­tion in re­sponse to changes in the lo­ca­tion of food. In an ex­per­i­ment with a T-maze, re­searchers trained ants to a feeder lo­ca­tion, then al­tered the en­vi­ron­ment by chang­ing the feeder lo­ca­tion to the other arm of the T-maze. After find­ing the new food source, ants up­reg­u­lated pheromone de­po­si­tion if they had made a wrong choice. Ad­di­tion­ally, the re­searchers found that out­go­ing ants which went on to make an er­ror de­posited less pheromone. This seems to im­ply that the ants can mea­sure the re­li­a­bil­ity of their own mem­o­ries, and re­spond ac­cord­ingly, de­posit­ing more or less pheromones.[39]

Uncer­tainty mon­i­tor­ing is a form of metacog­ni­tion. Ac­cord­ing to many higher-or­der the­o­ries of con­scious­ness, metacog­ni­tion is a nec­es­sary con­di­tion on con­scious ex­pe­rience. More spec­u­la­tively, metacog­ni­tion might be con­strued as a type of self-aware­ness. And self-aware­ness is plau­si­bly a suffi­cient con­di­tion on con­scious ex­pe­rience. (One must be con­scious in or­der to be self-con­scious.) Thus, un­cer­tainty mon­i­tor­ing is a par­tic­u­larly im­por­tant fea­ture to in­ves­ti­gate. In­deed, it has been said that “the com­par­a­tive study of metacog­ni­tion po­ten­tially grounds the sys­tem­atic study of an­i­mal con­scious­ness.”[40]

How­ever, one ought to in­ter­pret the alleged ex­am­ples of un­cer­tainty mon­i­tor­ing in in­ver­te­brates with cau­tion. Even the au­thors of such stud­ies are un­sure what their re­search rep­re­sents. Re­gard­ing their find­ings on the up­reg­u­la­tion of pheromone de­posits in ants, Tomer Cza­czkes and Jür­gen Heinze write, “it’s hard to be­lieve that such tiny-brained an­i­mals are ca­pa­ble of such an ad­vanced cog­ni­tive feat” and “one could con­ceive of sev­eral al­ter­na­tive ex­pla­na­tions for our find­ings, which do not in­voke metacog­ni­tion.” At the same time, they ar­gue that their find­ings, “alongside similar re­sults from hon­ey­bees (Perry & Bar­ron, 2013), are sug­ges­tive of metacog­ni­tive abil­ities in so­cial in­sects.”[41] As with many other fea­tures, more re­search is needed.

Self-recog­ni­tion (mir­ror test)

Self-recog­ni­tion is an im­por­tant fea­ture to in­ves­ti­gate be­cause if self-recog­ni­tion im­plies self-aware­ness, then on some the­o­ries of mind, self-recog­ni­tion is fairly di­rect ev­i­dence of con­scious­ness. Self-recog­ni­tion in non­hu­man an­i­mals is gen­er­ally mea­sured via the mir­ror test. The test as­sesses self-recog­ni­tion by de­ter­min­ing whether an an­i­mal can rec­og­nize its own re­flec­tion in a mir­ror. This is ac­com­plished by se­cretly mark­ing the an­i­mal with a small dot that is only visi­ble by look­ing in the mir­ror. If the an­i­mal sees the dot in the mir­ror then touches the dot on its body (in­di­cat­ing it un­der­stands the re­la­tion­ship be­tween it­self and the crea­ture in the mir­ror), it passes the test.

The mir­ror test has sev­eral well-known method­olog­i­cal short­com­ings. For ex­am­ple, be­cause the test uses vi­sual per­cep­tion, crea­tures which per­ceive the world pri­mar­ily through other sense modal­ities seem to be at a dis­ad­van­tage. (Dogs, who have re­peat­edly failed the clas­sic mir­ror test, nav­i­gate the world mostly by a com­bi­na­tion of ol­fac­tion and au­di­tion.) Crea­tures for whom eye con­tact is a sign of ag­gres­sion also seem to be at a dis­ad­van­tage be­cause they will ei­ther re­fuse to di­rectly in­ves­ti­gate their re­flec­tion, or, if they do make pro­tracted eye con­tact, will move to coun­ter­act the per­ceived ag­gres­sion of the ‘for­eign’ crea­ture be­fore they have an op­por­tu­nity to no­tice the dot. (Go­rillas, who are mostly re­ported to fail the mir­ror test, fit this pro­file.)

Th­ese flaws lead to false nega­tives.[42] But false pos­i­tives are also pos­si­ble. The mir­ror test is an im­perfect mea­sure of self-recog­ni­tion. But even if the mir­ror test were a perfect mea­sure, it would still be difficult in some cases to defini­tively say whether some an­i­mal passes the test. For in­stance, ac­cord­ing to a re­cent study, a species of bony fish (the bluestreak cleaner wrasse, Labroides dimi­di­a­tus) passes the mir­ror test, the first an­i­mal out­side birds and mam­mals to do so.[43] From our non-spe­cial­ist per­spec­tive, it is un­clear how to eval­u­ate such a new, con­tro­ver­sial find­ing, es­pe­cially given the small sam­ple size of the study.[44] Thus, for this fea­ture and many oth­ers, we have been forced to make some difficult judg­ment calls. Again, we have tried to in­di­cate as much in com­ments at­tached to the rele­vant cells.

Deception

De­cep­tive be­hav­ior in an­i­mals comes in a wide va­ri­ety of forms. Many species use mimicry or cam­ou­flage to avoid preda­tors or am­bush prey. Some species tem­porar­ily adopt more ag­gres­sive be­hav­ior dur­ing times of vuln­er­a­bil­ity to de­ter at­tack­ers. And some species, no­tably hu­mans, in­ten­tion­ally mis­rep­re­sent their be­liefs in or­der to achieve some goal.

For pur­poses of this pro­ject, we are only con­cerned with de­cep­tive be­hav­ior in­so­far as it bears on the pos­ses­sion of phe­nom­e­nal con­scious­ness. Thus, gen­uine de­cep­tion (also some­times called “tac­ti­cal” or “in­ten­tional” de­cep­tion) must be dis­t­in­guished from pas­sive adap­ta­tions, such as mimicry or cam­ou­flage. If pos­si­ble, gen­uine de­cep­tive be­hav­ior also ought to be dis­t­in­guished from be­hav­iors that ap­pear to be in­stances of de­cep­tion but are in fact in­nately speci­fied or au­to­mat­i­cally elic­ited by ex­ter­nal stim­uli. In prac­tice, of course, it may be difficult to make this dis­tinc­tion.[45]

Gen­uine de­cep­tion is a com­plex cog­ni­tive and so­cial skill. To de­ceive, one must be ca­pa­ble of ap­pre­ci­at­ing the dis­tinc­tion be­tween pre­tense and re­al­ity. One must also be ca­pa­ble of rep­re­sent­ing, to some ex­tent, the men­tal states of the de­cep­tion tar­get. To de­ceive one must have a cog­ni­tive grasp on how things ap­pear, both to one­self and to one’s tar­get. To be aware of ap­pear­ances, one must ex­pe­rience them. A com­plex form of be­hav­ior in which an an­i­mal uses ap­pear­ances to de­ceive other an­i­mals is thus po­ten­tially fairly di­rect ev­i­dence that the an­i­mal is phe­nom­e­nally con­scious. The ab­sence of de­cep­tive be­hav­ior, how­ever, doesn’t tell us much. Higher-or­der cog­ni­tion is plau­si­bly not a re­quire­ment for phe­nom­e­nal con­scious­ness.[46]

For a plau­si­ble ex­am­ple of gen­uine de­cep­tion in in­ver­te­brates, con­sider cut­tlefish. Cut­tlefish de­ploy a wide va­ri­ety of chro­matic, tex­tu­ral, pos­tu­ral, and lo­co­mo­tor el­e­ments to com­mu­ni­cate with preda­tors, prey, and con­speci­fics, and there is ev­i­dence that they pos­sess a so­phis­ti­cated the­ory of mind.[47] Dur­ing courtship male cut­tlefish en­gage in a re­mark­able form of tac­ti­cal de­cep­tion with ri­val males: si­mul­ta­neous dual gen­der sig­nal­ling.[48] A male will po­si­tion it­self be­tween a ri­val male and a po­ten­tial mate. On the side of its man­tle fac­ing the po­ten­tial mate, the de­cep­tive male will pro­duce typ­i­cal chro­matic courtship pat­terns. But on the side of its man­tle fac­ing the ri­val male, it will mimic typ­i­cal fe­male dis­plays, thus con­fus­ing the ri­val and sig­nifi­cantly re­duc­ing the odds that the ri­val male will at­tempt to dis­rupt cop­u­la­tion.

Tool use

It was once thought that only hu­mans use tools. Although the defi­ni­tion of “tool” ad­mits of bor­der­line cases and the phe­nomenon “us­ing a tool” is similarly vague, it has nev­er­the­less be­come clear that this old thought is false. A wide range of non­hu­man an­i­mals, in­clud­ing mam­mals, birds, even some fish,[49] use a va­ri­ety of tools to great effect.

Tool use is of­ten con­sid­ered a bench­mark of cog­ni­tive so­phis­ti­ca­tion. Gen­uine tool use re­quires the ac­qui­si­tion of a for­eign ob­ject to be uti­lized at some later time. (As such, the makeshift shells some­times ac­quired by her­mit crabs do not qual­ify as tool use be­cause the shell is effec­tively in use the whole time the crab in­hab­its it.) In most cases of tool use, the ac­qui­si­tion or trans­porta­tion of the tool in­flicts some cost on the an­i­mal, for which the an­i­mal is com­pen­sated by some benefit when the tool is later de­ployed. Thus, tool use also re­quires a cer­tain de­gree of fore­sight and plan­ning.[50]

For pur­poses of this re­port, we sep­a­rate mere tool use, which is of­ten in­stinc­tive and nar­rowly-struc­tured, from so-called “flex­ible” tool use. An an­i­mal is ca­pa­ble of flex­ible tool use when it can uti­lize ob­jects with which it does not have an evolu­tion­ary his­tory. Mere tool use, in con­trast, is con­fined to nat­u­ral ob­jects and nor­mally oc­curs only in re­sponse to spe­cific en­vi­ron­men­tal cues in or­der to achieve a small num­ber of spe­cific goals. Although ev­i­dence for flex­ible tool use in in­ver­te­brates is only just emerg­ing (see be­low), sim­ple tool use has long been doc­u­mented in in­sects, for ex­am­ple the many species of ant that use leaves to trans­port food.

Flex­ible tool use

Among non­hu­man an­i­mals, tool use is per­haps most strik­ing in chim­panzees, who use tools for ev­ery­thing from nut-crack­ing to in­sect-gath­er­ing. (In­deed, the sub­tle vari­a­tions in con­structed tools among differ­ent chim­panzee pop­u­la­tions are some­times said to con­sti­tute “cul­tural” differ­ences among the groups.) This sort of tool-mak­ing and tool-us­ing is prob­a­bly too com­plex to be the di­rect product of evolu­tion­ary forces. Rather, it is a byproduct of chim­panzees’ gen­eral in­tel­li­gence.[51]

New ev­i­dence has re­cently emerged that flex­ible tool use is not re­stricted to pri­mates. Though con­tro­ver­sial, flex­ible tool use is now some­times at­tributed to in­ver­te­brates. For ex­am­ple, Finn et al. 2009 re­ports soft-sed­i­ment dwelling oc­to­puses re­triev­ing co­conut shell halves dis­carded by the lo­cal hu­man pop­u­la­tion and later as­sem­bling the shell halves into pro­tec­tive shelters. The awk­ward man­ner in which the oc­to­puses must move while car­ry­ing these shells (the au­thors de­scribe it as “stilt-walk­ing”) rep­re­sents a cost in terms of en­ergy and in­creased pre­da­tion risk, which is only re­couped later when the shelves are suc­cess­fully as­sem­bled into a sur­face shelter or en­cap­su­lat­ing lair. Im­por­tantly, the only known source of these clean and lightweight shells is the coastal hu­man com­mu­ni­ties, and thus the oc­to­puses have not in­ter­acted with these items on an evolu­tion­ary timescale.[52]

It has even been sug­gested that bees are ca­pa­ble of us­ing tools flex­ibly. In a re­cent study Loukola et al. 2017 trained bum­ble bees to see that a ball could be used to dis­pense a re­ward. In sub­se­quent iter­a­tions of the ex­per­i­ment, the bees in­de­pen­dently learned to solve the task more effi­ciently by us­ing a ball po­si­tioned more closely to the tar­get, even when the ball was a differ­ent color. Such cog­ni­tive flex­i­bil­ity is the hal­l­mark of so­phis­ti­cated tool use.[53]

Fi­nally, it must be noted that tool use, no mat­ter how in­ge­nious, is not di­rect ev­i­dence of valenced ex­pe­rience or phe­nom­e­nal con­scious­ness. Rather, tool use is pos­i­tively cor­re­lated with cog­ni­tive so­phis­ti­ca­tion. For those that be­lieve cog­ni­tive so­phis­ti­ca­tion is a nec­es­sary con­di­tion on phe­nom­e­nal con­scious­ness (or that phe­nom­e­nal con­scious­ness is a byproduct of cog­ni­tive so­phis­ti­ca­tion), tool use is then in­di­rect ev­i­dence for such states.

Credits

This es­say is a pro­ject of Re­think Pri­ori­ties. It was writ­ten by Ja­son Schukraft with con­tri­bu­tions from Max Carpen­dale. Thanks to Kim Cud­ding­ton, Mar­cus A. Davis, Peter Hur­ford, and Daniela Wald­horn for helpful feed­back. If you like our work, please con­sider sub­scribing to our newslet­ter. You can see all our work to date here.

Notes


  1. Ver­te­brates con­sti­tute a sub­phy­lum in the phy­lum Chor­data. Cladis­ti­cally, it would be more pre­cise to speak of ‘chor­dates’ and ‘non-chor­dates.’ In us­ing the terms ‘ver­te­brates’ and ‘in­ver­te­brates’ we defer to com­mon us­age. How­ever, the num­ber of in­ver­te­brates in the phy­lum Chor­data is triv­ial com­pared to the num­ber of in­ver­te­brates out­side Chor­data, so com­mon us­age is not wholly in­ac­cu­rate. ↩︎

  2. We use the terms ‘sen­tience,’ ‘phe­nom­e­nal con­scious­ness,’ and ‘sub­jec­tive ex­pe­rience’ in­ter­change­ably. An or­ganism is sen­tient just in case there is some­thing it is like to be that or­ganism. ‘Valenced ex­pe­rience’ de­notes a proper sub­set of con­scious ex­pe­rience in which ex­pe­riences take on a pos­i­tive or nega­tive af­fect. All crea­tures with the ca­pac­ity for valenced ex­pe­rience are nec­es­sar­ily sen­tient, but not all sen­tient crea­tures nec­es­sar­ily have the ca­pac­ity for valenced ex­pe­rience. Note: ‘sen­tience’ gets used in differ­ent ways by differ­ent philo­soph­i­cal com­mu­ni­ties. In philos­o­phy of mind, the term is nor­mally used in its broad sense, to mean ‘phe­nom­e­nal con­scious­ness.’ (See, in­ter alia, this SEP ar­ti­cle on an­i­mal con­scious­ness.) In moral philos­o­phy, the term is nor­mally used in its nar­row sense, to mean ‘valenced ex­pe­rience.’ (See, in­ter alia, this SEP ar­ti­cle on the grounds of moral sta­tus.) We have adopted the philos­o­phy of mind us­age. ↩︎

  3. For an ex­am­ple of this in crabs, see Stu­art Barr and Robert W. El­wood. 2011. “No ev­i­dence of mor­phine anal­ge­sia to nox­ious shock in the shore crab, Carcinus mae­nas.” Be­havi­oural pro­cesses 86, no. 3: 340-344. ↩︎

  4. Alexan­dra L. Whit­taker and Gor­don S. Howarth. 2014. “Use of Spon­ta­neous Be­havi­our Mea­sures to Assess Pain in Lab­o­ra­tory Rats and Mice: How Are We Pro­gress­ing?Ap­plied An­i­mal Be­havi­our Science 151: 1-12. ↩︎

  5. T.C. Dan­bury, C. A. Weeks, J. P. Cham­bers, A. E. Water­man-Pear­son, and S. C. Kestin. 2000. “Self-Selec­tion of the Anal­gesic Drug Carpro­fen by Lame Broiler Chick­ens.” The Ve­teri­nary Record 146: 307-311. ↩︎

  6. Ju­lia Groen­ing, Dustin Ven­ini, and Mandyam V. Srini­vasan. 2017. “In Search of Ev­i­dence for the Ex­pe­rience of Pain in Honey­bees: A Self-Ad­minis­tra­tion Study.” Scien­tific Re­ports 7: 45825. ↩︎

  7. Udita Datta, Moira van Staaden, and Robert Hu­ber. 2008. “Crayfish Self-Ad­minister Am­phetamine in a Spa­tially Contin­gent Task.” Fron­tiers in Phys­iol­ogy Vol­ume 9, Ar­ti­cle 433. ↩︎

  8. Eirik Søvik, Jen­nifer L. Cor­nish, and An­drew B. Bar­ron. 2013. “Co­caine Tol­er­ance in Honey Bees.” PLoS ONE 8 (5): e64920. ↩︎

  9. D.A. No­ever, R.J. Cro­nise, and R.A. Relwani. 1995. “Us­ing Spi­der-Web Pat­terns To Deter­mine Tox­i­c­ity.” NASA Tech Briefs, 19 (4), 82. ↩︎

  10. Eric Eds­inger and Gül Dölen. 2018. “A Con­served Role for Sero­ton­er­gic Neu­ro­trans­mis­sion in Me­di­at­ing So­cial Be­hav­ior in Oc­to­pus.” Cur­rent Biol­ogy 28: P3136-314.E4. ↩︎

  11. See, for ex­am­ple, Brian V. Entler, J. Ti­mothy Can­non, and Marc A. Seid. 2016. “Mor­phine Ad­dic­tion in Ants: A New Model for Self-Ad­minis­tra­tion and Neu­ro­chem­i­cal Anal­y­sis.” The Jour­nal of Ex­per­i­men­tal Biol­ogy 219.18: 2865–69. ↩︎

  12. Stephen M. Top­per, Sara C. Aguilar, Vik­to­ria Y. Top­per, Erin El­bel, and Jonathan T. Pierce-Shi­mo­mura. 2014. “Al­co­hol dis­in­hi­bi­tion of be­hav­iors in C. el­e­gans.” PLoS One 9, no. 3: e92965. ↩︎

  13. This is the most com­mon paradigm for test­ing self-ad­minis­tra­tion, but there are other paradigms that are some­times used. For ex­am­ple, to test the self-ad­minis­tra­tion of am­phetamine in crayfish, re­searchers used a spa­tially con­tin­gent task paradigm in which the an­i­mals had to dis­t­in­guish a quad­rant of the arena with a par­tic­u­lar tex­tured sub­strate in or­der to earn the drug. Udita Datta, Moira van Staaden, and Robert Hu­ber. 2008. “Crayfish Self-Ad­minister Am­phetamine in a Spa­tially Contin­gent Task.” Fron­tiers in Phys­iol­ogy Vol­ume 9, Ar­ti­cle 433. ↩︎

  14. Kent C. Ber­ridge and Terry E. Robin­son. 2011. “Drug Ad­dic­tion as In­cen­tive Sen­si­ti­za­tion.” in Poland and Gra­ham (eds.) Ad­dic­tion and Re­spon­si­bil­ity MIT Press: 21-54. ↩︎

  15. An anx­iolytic drug is a med­i­ca­tion used to treat anx­iety. ↩︎

  16. Ari­ane-Saskia Ries, Tim Her­manns, Burkhard Poeck, and Roland Strauss. 2017. “Sero­tonin mod­u­lates a de­pres­sion-like state in Drosophila re­spon­sive to lithium treat­ment.” Na­ture Com­mu­ni­ca­tions 8, Ar­ti­cle num­ber: 15738. ↩︎

  17. Alex T. Ford and Peter P. Fong. 2015. “The Effects of An­tide­pres­sants Ap­pear to Be Rapid and at En­vi­ron­men­tally Rele­vant Con­cen­tra­tions.” En­vi­ron­men­tal Tox­i­col­ogy and Chem­istry, 35(4), 794-798. ↩︎

  18. Trevor James Hamil­ton, Garfield T. Kwan, Joshua Gal­lup and Martin Tres­guer­res. 2016. “Acute fluox­e­tine ex­po­sure al­ters crab anx­iety-like be­havi­our, but not ag­gres­sive­ness.” Scien­tific Re­ports vol­ume 6, Ar­ti­cle num­ber: 19850. ↩︎

  19. Even in hu­mans, an­tide­pres­sants and anx­iolyt­ics can some­times cause a wide range of un­pleas­ant side effects. See James M Fer­gu­son. 2001. “SSRI an­tide­pres­sant med­i­ca­tions: ad­verse effects and tol­er­abil­ity.” Pri­mary care com­pan­ion to the Jour­nal of clini­cal psy­chi­a­try 3, no. 1: 22-27 and J. Guy Ed­wards. 1981. “Ad­verse effects of an­ti­anx­iety drugs.” Drugs 22, no. 6: 495-514. ↩︎

  20. Pas­cal Fos­sat, Julien Bac­qué-Cazenave, Philippe De Deur­waerdère, Jean-Paul Delbecque, and Daniel Cat­taert. 2014. “Anx­iety-like be­hav­ior in crayfish is con­trol­led by sero­tonin.” Science 344, no. 6189: 1293-1297. Note that the pop­u­lar in­tro­duc­tion to the ar­ti­cle mis­tak­enly states that the crayfish were afraid of the dark, not the light. A cor­rected ti­tle for the pop­u­lar in­tro­duc­tion is available here. ↩︎

  21. Separately, the in­jec­tion of sero­tonin in un­shocked crayfish in­duced light-aver­sion be­hav­ior that was also elimi­nated by chlor­diazepox­ide. In hu­mans, ele­vated lev­els of sero­tonin are as­so­ci­ated with anx­iety. ↩︎

  22. This fea­ture is of­ten in­ves­ti­gated us­ing the con­di­tioned prefer­ence paradigm, which is usu­ally used for study­ing drug ad­dic­tions in an­i­mals. Th­ese ex­per­i­ments have been widely de­vel­oped with rats. See, e.g., Thomas M. Tzschen­tke. 1998. “Mea­sur­ing re­ward with the con­di­tioned place prefer­ence paradigm: a com­pre­hen­sive re­view of drug effects, re­cent progress and new is­sues.” Progress in Neu­ro­biol­ogy 56, no. 6: 613-672. ↩︎

  23. Karla R. Kaun, Anita V. Dev­i­neni, and Ulrike He­ber­lein. 2012. “Drosophila melanogaster as a model to study drug ad­dic­tion.” Hu­man ge­net­ics 131, no. 6: 959-975. ↩︎

  24. The con­tin­gen­cies un­der which a re­in­forcer is pre­sented, rather than (or in ad­di­tion to) its phys­i­cal prop­er­ties, can in­fluence whether or not an as­so­ci­a­tion is gen­er­ated. This is called “se­lec­tive as­so­ci­a­tion.” See, in­ter alia, Stan­ley J. Weiss, Leigh V. Pan­lilio, and Charles W. Sch­indler. 1993. “Selec­tive as­so­ci­a­tions pro­duced solely with ap­pet­i­tive con­tin­gen­cies: The stim­u­lus‐re­in­forcer in­ter­ac­tion re­vis­ited.” Jour­nal of the Ex­per­i­men­tal Anal­y­sis of Be­hav­ior 59, no. 2: 309-322. Ad­di­tion­ally, in stud­ies with ver­te­brates, it has been seen that an an­i­mal’s perfor­mance in a con­di­tion­ing ex­per­i­ment may be af­fected by the choice of par­tic­u­lar com­bi­na­tions of con­di­tioned or dis­crim­i­na­tive stim­uli and re­in­forcers. In other words, cer­tain com­bi­na­tions of stim­uli and re­in­forcers may fail to elicit ex­pected be­hav­iors, whereas other com­bi­na­tions from the same set of stim­uli do re­sult in the ex­pected perfor­mance. This is called “stim­u­lus-re­in­forcer in­ter­ac­tion.” See, in­ter alia, Don­ald D. Foree and Vin­cent M. LoLordo. 1973. “At­ten­tion in the pi­geon: differ­en­tial effects of food-get­ting ver­sus shock-avoidance pro­ce­dures.” Jour­nal of Com­par­a­tive and Phys­iolog­i­cal Psy­chol­ogy 85, no. 3: 551. ↩︎

  25. Barry Magee and Robert El­wood. 2013. “Shock avoidance by dis­crim­i­na­tion learn­ing in the shore crab (Carcinus mae­nas) is con­sis­tent with a key crite­rion for pain.” Jour­nal of Ex­per­i­men­tal Biol­ogy 216: 353-358. ↩︎

  26. Adele Di­a­mond. 2013. “Ex­ec­u­tive Func­tions.” An­nual re­view of psy­chol­ogy 64: 135-168. ↩︎

  27. Young chil­dren and chim­panzees rou­tinely fail tests of self-con­trol. Chil­dren be­gin to out­perform chimps around age six. Es­ther Her­rmann, An­to­nia Misch, Vic­to­ria Her­nan­dez‐Lloreda, and Michael To­masello. 2015. “Uniquely hu­man self‐con­trol be­gins at school age.” Devel­op­men­tal sci­ence 18, no. 6: 979-993. ↩︎

  28. Ken Cheng,, Jen­nifer Peña, Me­lanie A. Porter, and Ju­lia D. Ir­win. 2002. “Self-Con­trol in Honey­bees.” Psy­cho­nomic Bul­letin & Re­view 9: 259-263. ↩︎

  29. Pawan­deep Sandhu, Oskar Shura, Ros­al­ind L. Mur­ray, and Cylita Guy. 2018. “Worms make risky choices too: the effect of star­va­tion on for­ag­ing in the com­mon earth­worm (Lum­bri­cus ter­restris).” Cana­dian Jour­nal of Zool­ogy 96, no. 11: 1278-1283. ↩︎

  30. William T. Gib­son, Car­los R. Gon­za­lez, Conchi Fer­nan­dez, Lak­sh­mi­narayanan Ra­masamy, Tanya Tabach­nik, Re­becca R. Du, Panna D. Fel­sen, Michael R. Maire, Pietro Perona, and David J. An­der­son. 2015. “Be­hav­ioral re­sponses to a repet­i­tive vi­sual threat stim­u­lus ex­press a per­sis­tent state of defen­sive arousal in Drosophila.” Cur­rent Biol­ogy 25, no. 11: 1401-1415. ↩︎

  31. Barry Magee and Robert El­wood. 2016. “Trade-offs be­tween preda­tor avoidance and elec­tric shock avoidance in her­mit crabs demon­strate a non-re­flex­ive re­sponse to nox­ious stim­uli con­sis­tent with pre­dic­tion of pain.” Be­havi­oural Pro­cesses 130: 31-35. ↩︎

  32. It should also be noted that for some species, such as sheep and cat­tle, anti-preda­tor re­sponses are no longer needed, and thus are no longer adap­tive, due to do­mes­ti­ca­tion. Cor­nelia Flör­cke and Tem­ple Grandin. 2013. “Loss of anti-preda­tor be­hav­iors in cat­tle and the in­creased pre­da­tion losses by wolves in the North­ern Rocky Moun­tains.” Open Jour­nal of An­i­mal Sciences 3, no. 03: 248. ↩︎

  33. Sam C.C. Chan, Chetwyn C.H. Chan, Anne S.K. Kwan, Kin-hung Ting, and Tak-yi Chui. 2012. “Ori­ent­ing at­ten­tion mod­u­lates pain per­cep­tion: an ERP study.” PLoS One 7, no. 6: e40215. ↩︎

  34. C. H. Eise­mann, W. K. Jor­gensen, D. J. Mer­ritt, M. J. Rice, B. W. Cribb, P. D. Webb and M. P. Zalucki. 1984. “Do In­sects Feel Pain? - A Biolog­i­cal View.” Ex­per­en­tia 40: 164-167. ↩︎

  35. Alter­na­tively, it might ex­pe­rience the pro­cess of mat­ing as so im­mensely plea­surable that the pain of be­ing eaten al­ive is out­weighed. ↩︎

  36. Kristen E. Lyons and Si­mona Ghetti. 2011. “The de­vel­op­ment of un­cer­tainty mon­i­tor­ing in early child­hood.” Child Devel­op­ment 82, no. 6 : 1778-1787. ↩︎

  37. Michael J.Beran, Justin J. Couch­man, Mar­i­ana VC Coutinho, Joseph Boomer, and J. David Smith. 2010. “Me­tacog­ni­tion in non­hu­mans: method­olog­i­cal and the­o­ret­i­cal is­sues in un­cer­tainty mon­i­tor­ing.” In Efk­lides A., Mi­sailidi P. (eds)Trends and Prospects in Me­tacog­ni­tion Re­search, pp. 21-35. Springer, Bos­ton, MA. ↩︎

  38. Clint J. Perry and An­drew B. Bar­ron. 2013. “Honey bees se­lec­tively avoid difficult choices.” Pro­ceed­ings of the Na­tional Academy of Sciences 110, no. 47: 19155-19159. ↩︎

  39. Tomer J. Cza­czkes and Jür­gen Heinze. 2015. “Ants ad­just their pheromone de­po­si­tion to a chang­ing en­vi­ron­ment and their prob­a­bil­ity of mak­ing er­rors.” Pro­ceed­ings of the Royal So­ciety B: Biolog­i­cal Sciences 282, no. 1810: 20150679. ↩︎

  40. J. David Smith, Wendy E. Shields, and David A. Wash­burn. 2003. “The com­par­a­tive psy­chol­ogy of un­cer­tainty mon­i­tor­ing and metacog­ni­tion.” Be­hav­ioral and Brain Sciences 26, no. 3: 317-339. ↩︎

  41. Cza­czkes and Heinze 2015: 5. ↩︎

  42. False nega­tives are even found in six-year-old hu­mans. At least one study in­di­cates the av­er­age age at which chil­dren first pass the mir­ror test varies con­sid­er­ably across cul­tures. One hy­poth­e­sis is that non-Western chil­dren use mir­rors less fre­quently and less con­spicu­ously than their Western peers. Thus, al­though non-Western chil­dren ac­quire the self-con­cept at roughly the same de­vel­op­ment stage as their Western coun­ter­parts, mir­ror use, es­pe­cially pub­lic mir­ror use, con­fuses them. Tanya Broesch, Tara Cal­laghan, Joseph Hen­rich, Chris­tine Mur­phy, and Philippe Rochat. 2011. “Cul­tural vari­a­tions in chil­dren’s mir­ror self-recog­ni­tion.” Jour­nal of Cross-Cul­tural Psy­chol­ogy 42, no. 6: 1018-1029. ↩︎

  43. Masanori Ko­hda, Takashi Hotta, To­mo­hiro Takeyama, Satoshi Awata, Hirokazu Tanaka, Jun-ya Asai, and Alex L. Jor­dan. 2019. “If a fish can pass the mark test, what are the im­pli­ca­tions for con­scious­ness and self-aware­ness test­ing in an­i­mals?.” PLoS Biol­ogy 17, no. 2: e3000021. ↩︎

  44. For a crit­i­cal re­sponse, see Frans B. M. de Waal. 2019. “Fish, Mir­rors, and a Grad­u­al­ist Per­spec­tive on Self-Aware­ness.” PLoS Biol­ogy 17, no. 2: e3000112. ↩︎

  45. Stan Kuczaj, Karissa Tranel, Marie Trone, and Heather Hill.. 2001. “Are An­i­mals Ca­pable of De­cep­tion or Em­pa­thy? Im­pli­ca­tions for An­i­mal Con­scious­ness and An­i­mal Welfare.” An­i­mal Welfare 10: 161-173. ↩︎

  46. Michael Tye. 2017. “Do Fish Have Feel­ings?” in Kristen An­drews and Ja­cob Beck (eds.) The Rout­ledge Hand­book of Philos­o­phy of An­i­mal Minds 169-175. ↩︎

  47. Am­ber Thomas and Christy MacDon­ald. 2016. “In­ves­ti­gat­ing body pat­tern­ing in aquar­ium-raised flam­boy­ant cut­tlefish (Me­tasepia pfefferi).” PeerJ 4: e2035. ↩︎

  48. Cu­lum Brown, Martin P. Gar­wood, and Jane E. Willi­am­son. 2012. “It Pays to Cheat: Tac­ti­cal De­cep­tion in a Cephalo­pod So­cial Sig­nal­ling Sys­tem.” Biol­ogy Let­ters 8: 729-732. ↩︎

  49. Gi­a­como Bernardi. 2012. “The use of tools by wrasses (Labri­dae).” Co­ral Reefs 31, no. 1: 39. ↩︎

  50. Christo­pher Baber. 2003. Cog­ni­tion and Tool Use: Forms of En­gage­ment in Hu­man and An­i­mal Use of Tools. Lon­don: CRC Press. ↩︎

  51. William C. McGrew. 1992. Chim­panzee Ma­te­rial Cul­ture: Im­pli­ca­tions for Hu­man Evolu­tion. Cam­bridge Univer­sity Press. ↩︎

  52. Ju­lian K. Finn, Tom Tre­genza, and Mark D. Nor­man. 2009. “Defen­sive Tool Use in a Co­conut-Car­ry­ing Oc­to­pus.” Cur­rent Biol­ogy 19: PR1069-0R1070. ↩︎

  53. Olli J. Loukola, Clint J. Perry, Louie Coscos, and Lars Chit­tka. 2017. “Bum­ble­bees Show Cog­ni­tive Flex­i­bil­ity by Im­prov­ing on an Ob­served Com­plex Be­hav­ior.” Science 355: 833-836. (See here for an in­ex­pli­ca­bly adorable video clip of the bees in ac­tion.) ↩︎